Altered host plant preference of Tetranychus urticae and prey preference of its predator Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae) on transgenic Cry3Bb-eggplants

The behavior of the two-spotted spider mite, Tetranychus urticae Koch and the predatory mite Phytoseiulus persimilis A.-H. was investigated in laboratory experiments with transgenic Bt-eggplants, Solanum melongena L., producing the Cry3Bb toxin and corresponding isogenic, non-transformed eggplants. In bitrophic experiments, dual-choice disc tests were conducted to reveal the effects of transgenic eggplants on host plant preference of T. urticae. Adult spider mite females were individually placed on leaf discs (2 cm diameter) and were observed during five days. Females occurred significantly more frequently on transgenic halves on which also significantly more T. urticae eggs were found. The effects of a Cry3Bb-eggplant fed prey on the feeding preference of P. persimilis were investigated in tritrophic experiments. Sixteen spider mite females, eight of which had been taken from transgenic and eight from isogenic eggplants, were offered to well-fed females of P. persimilis and numbers of respective spider mites consumed were registered 12 h later when the predators were offered new spider mites again. This procedure was repeated six times. The results revealed that predatory mites consumed significantly less Bt-fed spider mites than prey that had been raised on control eggplants. These results indicate that eggplants expressing the Cry3Bb toxin for resistance against the Colorado potato beetle are more preferred by spider mites but are less preferred by their predator P. persimilis. Possible consequences of these findings for biological control of spider mites on eggplants are discussed.     

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.     

PCR-based identification of the pathogenic bacterium, Acaricomes phytoseiuli, in the biological control agent Phytoseiulus persimilis (Acari: Phytoseiidae)

The predatory mite, Phytoseiulus persimilis is an important biological control agent of herbivorous spider mites. This species is also intensively used in the study of tritrophic effects of plant volatiles in interactions involving plants, herbivores, and their natural enemies. Recently, a novel pathogenic bacterium, Acaricomes phytoseiuli, has been isolated from adult P. persimilis females. This pathogen causes a characteristic disease syndrome with dramatic changes in longevity, fecundity, and behavior. Healthy P. persimilis use spider mite-induced volatiles to locate prey patches. Infection with A. phytoseiuli strongly reduces the attraction to herbivore-induced plant volatiles. The loss of response to herbivore-induced plant volatiles along with the other disease symptoms can have a serious impact on the success of biological control of spider mites. In this study, we have developed a molecular tool (PCR) to detect the pathogenic bacterium in individual predatory mites. PCR primers specific for A. phytoseiuli were developed based on 16S ribosomal DNA of the bacterium. The PCR test was validated with DNA extracted from predatory mites that had been exposed to A. phytoseiuli. A survey on different P. persimilis populations as well as other predatory mite species from several companies that rear predatory mites for biological control revealed that the disease is widespread in Europe and is restricted to P. persimilis. The possibility that the predatory mites get infected via their prey Tetranychus urticae could be eliminated since the PCR test run on prey gave a negative result.     

Effects of feeding frequency and sugar concentration on behavior and longevity of the adult aphid parasitoid: Aphidius ervi (Haliday) (Hymenoptera: Braconidae)

The effectiveness of the predatory mite, Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae), as a suppressive agent of the twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), was evaluated on greenhouse ivy geraniums at predator:prey release ratios of 1:60, 1:20, and 1:4. Releases at each predator:prey ratio were made at moderate and high T. urticae densities to determine if initial pest population size influenced the suppressive ability of the predator. At ratios of 1:4 and 1:20, P. persimilis significantly reduced T. urticae populations 1 week after release and kept them at low levels thereafter. Plant damage also was significantly reduced at these densities. After 4 weeks, the P. persimilis that were released at a ratio of 1:4 consistently reduced T. urticae populations from densities as high as 30 T. urticae per leaf to fewer than 0.6 per leaf. We found no interaction between release ratio and T. urticae density, indicating that predator effectiveness remains constant, at least within the range of T. urticae densities used. Our work demonstrates the potential of P. persimilis to provide effective control of T. urticae on a greenhouse-grown floricultural crop at a moderately low predator:prey ratio (1:20) and over a range of initial pest densities. However, we recommend that P. persimilis be released at a ratio of 1:4 for greatest reliability and successful control of T. urticae on ivy geraniums.     

Comparative toxicity of some acaricides to the predatory mite, Phytoseiulus persimilis and the twospotted spider mite, Tetranychus urticae

The relative toxicity of someacaricides to the predatory mite, Phytoseiulus persimilis and the twospottedspider mite, Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) wasevaluated in laboratory. Five of theacaricides tested, including bifenazate,acequinocyl, chlorfenapyr, flufenoxuron andfenbutatin oxide, were much less toxic to adultfemales and immatures of P. persimilisthan to those of T. urticae, and adultfemale predators treated with these fiveacaricides produced 84±96% as many eggs as didcontrol females. Etoxazole did not seriouslyaffect the survival and reproduction of adultfemale predators but caused high mortalityrates in eggs and larvae of P.persimilis. Milbemectin and fenazaquin werevery toxic to adult females and immatures ofP. persimilis. Adult female predatorssurvived on a diet of spider mites treated withbifenazate, acequinocyl, chlorfenapyr,flufenoxuron and fenbutatin oxide, and theirfecundity, prey consumption and the sex ratioof the progeny were not substantially affected. Based on the results, bifenazate, acequinocyl,chlorfenapyr, flufenoxuron and fenbutatin oxideappeared to be the promising candidates for usein integrated mite management programs whereP. persimilis is the major naturalenemy.     

Allocating time between feeding, resting and moving by the two-spotted spider mite, Tetranychus urticae and its predator Phytoseiulus persimilis

This study characterizes the timing of feeding, moving and resting for the two-spotted spider mite, Tetranychus urticae Koch and a phytoseiid predator, Phytoseiulus persimilis Athias-Henriot. Feeding is the interaction between T. urticae and plants, and between P. persimilis and T. urticae. Movement plays a key role in locating new food resources. Both activities are closely related to survival and reproduction. We measured the time allocated to these behaviours at four ages of the spider mite (juveniles, adult females immediately after moult and adult females 1 and 3 days after moult) and two ages of the predatory mite (juveniles and adult females). We also examined the effect of previous spider mite-inflicted leaf damage on the spider mite behaviour. Juveniles of both the spider mite and the predatory mite moved around less than their adult counterparts. Newly emerged adult female spider mites spent most of their time moving, stopping only to feed. This represents the teneral phase, during which adult female spider mites are most likely to disperse. With the exception of this age group, spider mites moved more and fed less on previously damaged than on clean leaves. Because of this, the spider mite behaviour was initially more variable on damaged leaves. Phytoseiulus persimilis rested at all stages for a much larger percentage of the time and spent less time feeding than did T. urticae; the predators invariably rested in close proximity to the prey. Compared to adult predators, juveniles spent approximately four times as long handling a prey egg. The predator-prey interaction is dependent upon the local movement of both the predators and prey. These details of individual behaviours in a multispecies environment can provide an understanding of population dynamics.     

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.     

Do spider mite-infested plants and spider mite trails attract predatory mites?

We questioned the well-accepted concept that spider mite-infested plants attract predatory mites from a distance. This idea is based on the preference demonstrated by predatory mites such as Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) for volatiles produced by spider mite-infested plants in a closed environment (Y-tube wind tunnel). However, in natural open environments, kidney bean leaves heavily infested with Tetranychus urticae Koch (Acari: Tetranychidae) did not attract P. persimilis from the same distances as were used in the Y-tube tests. Therefore, the attraction of predatory mites for spider mite-infested plant volatiles in the Y-tube tests may reflect a preference in a closed environment and should be carefully interpreted as a basis for extrapolating predator–prey attraction mechanisms in the wild. On the other hand, we showed that adult female P. persimilis could follow trails laid down by adult female T. urticae in the laboratory and in natural open environments. Consequently, we propose that following spider mite trails represents another prey-searching cue for predatory mites.     

Phytoseiulus persimilis response to herbivore-induced plant volatiles as a function of mite-days

The predatory mite, Phytoseiulus persimilis (Acari: Phytoseiidae), uses plant volatiles (i.e., airborne chemicals) triggered by feeding of their herbivorous prey, Tetranychus urticae (Acari: Tetranychidae), to help locate prey patches. The olfactory response of P. persimilis to prey-infested plants varies in direct relation to the population growth pattern of T. urticae on the plant; P. persimilis responds to plants until the spider mite population feeding on a plant collapses, after which infested plants do not attract predators. It has been suggested that this represents an early enemy-free period for T. urticae before the next generation of females is produced. We hypothesize that the mechanism behind the diminished response of predators is due to extensive leaf damage caused by T. urticae feeding, which reduces the production of volatiles irrespective of the collapse of T. urticae population on the plant. To test this hypothesis we investigated how the response of P. persimilis to prey-infested plants is affected by: 1) initial density of T. urticae, 2) duration of infestation, and 3) corresponding leaf damage due to T. urticae feeding. Specifically, we assessed the response of P. persimilis to plants infested with two T. urticae densities (20 or 40 per plant) after 2, 4, 6, 8, 10, 12 or 14 days. We also measured leaf damage on these plants. We found that predator response to T. urticae-infested plants can be quantified as a function of mite-days, which is a cumulative measure of the standing adult female mite population sampled and summed over time. That is, response to volatiles increased with increasing numbers of T. urticae per plant or with the length of time plant was infested by T. urticae, at least as long at the leaves were green. Predatory mites were significantly attracted to plants that were infested for 2 days with only 20 spider mites. This suggests that the enemy-free period might only provide a limited window of opportunity for T. urticae because relatively low numbers of T. urticae per plant can attract predators. Leaf damage also increased as a function of mite-days until the entire leaf was blanched. T. urticae populations decreased at this time, but predator response to volatiles dropped before the entire leaf was blanched and before the T. urticae population decreased. This result supports our hypothesis that predator response to plant volatiles is linked to and limited by the degree of leaf damage, and that the quantitative response to T. urticae populations occurs only within a range when plant quality has not been severely compromised.     

Interactions among phytophagous mites, and introduced and naturally occurring predatory mites, on strawberry in the UK

In choice test experiments on strawberry leaf disc arenas the phytoseiid mites Neoseiulus californicus and N. cucumeris were more effective than Typhlodromus pyri as predators of the phytophagous mites Tetranychus urticae and Phytonemus pallidus. There were no preferences shown for either prey by any of these predators. In multiple predator leaf disc experiments both Phytoseiulus persimilis and N. cucumeris significantly reduced numbers of T. urticae eggs and active stages; this effect was seen when the two species were present alone or in combination with other predator species. Neoseiulus californicus was less effective at reducing T. urticae numbers, and T. pyri was not effective; no interaction between predator species was detected in these experiments. When T. urticae alone was present as prey on potted plants, P. persimilis and N. californicus were the only phytoseiids to significantly reduce T. urticae numbers. These two predator species provided effective control of T. urticae when P. pallidus was also present; however, none of the predators reduced numbers of P. pallidus. There were no significant negative interactions when different species of predators were present together on these potted plants. In field experiments, releases of both P. persimilis and N. cucumeris significantly reduced T. urticae numbers. However, there was a significant interaction between these predator species, leading to poorer control of T. urticae when both species were released together. These results show the importance of conducting predator/prey feeding tests at different spatial scales.     

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.     

Local and distant prey-related cues influence when an acarine predator leaves a prey patch

Over relatively long distances, the predatory mite Phytoseiulus persimilis is able to detect volatiles produced by bean plants that are infested by its prey, Tetranychus urticae, the twospotted spider mite. Our investigation examined the separate and combined effects of prey, their products, and prey-induced plant volatiles on when P. persimilis left a potential prey host plant. In wind tunnels, we assessed the relative importance of and interaction among local and distant prey-related cues. The examination of local cues included: (1) all local cues (prey eggs, webbing, and prey-induced plant volatiles), (2) food (prey eggs) and webbing only, (3) plant volatiles only, and (4) no prey-related cues. The examination of distant cues involved the presence or absence of prey-induced plant volatiles from upwind plants. External volatile cues, produced by placing prey-infested plants upwind in the wind tunnel, resulted in more predators leaving downwind plants, and leaving sooner, than when clean plants were upwind, regardless of the availability of prey or prey-related cues on the local plant. However, local cues, especially the presence of food/webbing, had a greater effect than distant cues on timing of predator leaving. Predators remained in larger numbers and for longer times on prey-infested plants. However, the presence of either locally-produced plant volatiles or food/webbing alone still reduced the number of predators leaving a plant in the first hour compared to clean plants. After the first hour, the number of predators leaving was primarily driven by the presence of food/webbing. When no food/webbing was available, predators left plants rapidly; if food/webbing was available, some predatory mites remained on plants at least 24 hours. Even if no food/webbing was available, predators presented with local volatiles remained on plants for several hours longer than on clean plants without local volatiles. These small changes in leaving rates may lead to differences in local population dynamics, and possibly regional persistence, of the predator-prey interaction in patchy environments.     

The Effects of Prey Patchiness, Predator Aggregation, and Mutual Interference on the Functional Response of Phytoseiulus persimilis Feeding on Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae)

The spatial distributions of two-spotted spider mites Tetranychus urticae and their natural enemy, the phytoseiid predator Phytoseiulus persimilis, were studied on six full-grown cucumber plants. Both mite species were very patchily distributed and P. persimilis tended to aggregate on leaves with abundant prey. The effects of non-homogenous distributions and degree of spatial overlap between prey and predators on the per capita predation rate were studied by means of a stage-specific predation model that averages the predation rates over all the local populations inhabiting the individual leaves. The empirical predation rates were compared with predictions assuming random predator search and/or an even distribution of prey. The analysis clearly shows that the ability of the predators to search non-randomly increases their predation rate. On the other hand, the prey may gain if it adopts a more even distribution when its density is low and a more patchy distribution when density increases. Mutual interference between searching predators reduces the predation rate, but the effect is negligible. The stage-specific functional response model was compared with two simpler models without explicit stage structure. Both unstructured models yielded predictions that were quite similar to those of the stage-structured model.     

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.     

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.     

Influences of the method of introduction of prey (Tetranychus urticae) and predators (Phytoseiulus persimilis) on the development of plant injury in tomato crops under glass

Two variants of the pest in first method of introduction of prey (Tetranychus urticae Koch) and predators (Phytoseiulus persimilis Athias-Henriot) on tomato crops were compared in a 80 m² glasshouse. As opposed to the second crop, the first crop was protected against spider mites by early and multiple releases of predators ensuring high spatial coincidence between prey and predators. Plant injury gradually increased in crop 1, whereas it first peaked and then decreased to low values in crop 2. Mean plant injury was higher in the former crop, and so was the degree of spatial variability. The lack of persistent control in crop 1 indicates that the predators suppressed, but did not annihilate the spider mites in the prey patches where the predators were introduced. This enabled the spider mites to resurge shortly after their enemies had disappeared due to lack of food. In crop 2, the way the biological control was conducted permitted the predators to achieve so high densities that they could annihilate the spider mites in most patches. Not only did this synchronize the prey populations but it also prevented the pest from a fast recovery. Moreover, predators did not disappear and maintained spider mite populations at low levels.     

Predation by Allothrombium pulvinum on the spider mites Tetranychus urticae and Amphitetranychus viennensis: Predation Rate, Prey Preference and Functional Response

The deutonymphs of Allothrombium pulvinum Ewing (Acari: Trombidiidae) are among the most important natural enemies of spider mites in North, North East and West Iran. In this study, maximum predation rate and preference experiments were conducted with A. pulvinum deutonymphs on apple leaf discs, to determine their preference for either of two spider mite species: Amphitetranychus viennensis (Zacher) and Tetranychus urticae Koch (Acari: Tetranychidae). Maximum predation rate tests showed that the predatory mite consumed more eggs and females of T. urticae than of A. viennensis. Furthermore, the Manly’s preference index for eggs and females of T. urticae confirmed that T. urticae were the preferred prey. The functional response of A. pulvinum deutonymphs on females of T. urticae was examined over a 24-h period. Predation of A. pulvinum deutonymphs presented with females of T. urticae followed a type III functional response. Estimated handling time for the predatory mites was 4.51 h and attack coefficient b, which describes the changes in attack rate with prey densities in a type III functional response, was 0.021.     

The Predatory Mite Phytoseiulus persimilis Adjusts Patch-leaving to Own and Progeny Prey Needs

Integration of optimal foraging and optimal oviposition theories suggests that predator females should adjust patch leaving to own and progeny prey needs to maximize current and future reproductive success. We tested this hypothesis in the predatory mite Phytoseiulus persimilis and its patchily distributed prey, the two-spotted spider mite Tetranychus urticae. In three separate experiments we assessed (1) the minimum number of prey needed to complete juvenile development, (2) the minimum number of prey needed to produce an egg, and (3) the ratio between eggs laid and spider mites left when a gravid P. persimilis female leaves a patch. Experiments (1) and (2) were the pre-requirements to assess the fitness costs associated with staying or leaving a prey patch. Immature P. persimilis needed at least 7 and on average 14±3.6 (SD) T. urticae eggs to reach adulthood. Gravid females needed at least 5 and on average 8.5±3.1 (SD) T. urticae eggs to produce an egg. Most females left the initial patch before spider mite extinction, leaving prey for progeny to develop to adulthood. Females placed in a low density patch left 5.6±6.1 (SD) eggs per egg laid, whereas those placed in a high density patch left 15.8±13.7 (SD) eggs per egg laid. The three experiments in concert suggest that gravid P. persimilis females are able to balance the trade off between optimal foraging and optimal oviposition and adjust patch-leaving to own and progeny prey needs.     

Diapause incidence in the two-spotted spider mite increases due to predator presence, not due to selective predation

We recently reported evidence for increased diapause incidence in the spider mite Tetranychus urticae in presence of the predatory mite Typhlodromus pyri. This effect may arise from (1) selective predation on non-diapause spider mites, (2) predator-induced diapause in spider mites, or (3) both. Using a different strain of T. urticae, we first recovered increased diapause incidence in association with predators. Then, we tested for selective feeding in two-choice experiments with equal numbers of non-diapause and diapause spider mites. We found that the predatory mite had a significant preference for the latter. This indicates that increased diapause incidence in association with predatory mites is not due to selective predation. Therefore, predator-mediated physiological induction of diapause seems a more likely explanation. The cues leading to induction appear to relate to the predators, not their effects, since predation simulated by spider-mite removal or puncturing did not significantly affect diapause incidence. Why spider mites benefit from this response, remains an open question.This revised version was published online in May 2005 with a corrected cover date.     

Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae)

The commercially available strains of Phytoseiulus persimilis Athias-Henriot, the biological control agent of Tetranychus urticae Koch, perform poorly in the Western Mediterranean, probably because they are not well adapted to local climatic conditions. For that reason, efforts are being focused on the development of a biological control programme using native phytoseiid mites. Four species of red spider mites can be found in vegetable crops in eastern Spain: T. urticae, Tetranychus turkestani Ugarov and Nikolski, Tetranychus ludeni Zacher and the recently introduced Tetranychus evansi Baker and Pritchard. To evaluate their potential role as biological control agents, the present study evaluates the life-history of local populations of Neoseiulus californicus (McGregor) and P. persimilis when fed on T. urticae, T. turkestani, T. evansi, and T. ludeni in the laboratory. Results indicate that N. californicus and P. persimilis are able to feed and complete their development on the four tested red spider mite species. The predators may exhibit a particularly high capacity for population increase when fed on T. urticae, T. turkestani, and T. ludeni, thus may be able to provide effective control of these species in the field. When fed T. evansi, however, predator performance was poor; significant increase in development and preoviposition times, and a reduction in oviposition period and fecundity were recorded. The resultant low capacity for population growth suggests poor ability of the two tested predators to suppress T. evansi populations on commercial crops. It is unlikely therefore that P. persimilis and N. californicus, now being widely used to control T. urticae in greenhouse crops in Central Europe, will be able to halt any spread of T. evansi to greenhouse crops in temperate areas.