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.     

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.     

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.     

Mite pests and their predators on seven vegetable crops (Arachnida: Acari)

During this study the frequency of occurrence and dominance of phytophagous and predatory mites harboring seven vegetable crops in Egypt, namely common bean, cowpea, eggplant, okra, squash, sweet pepper and sweet potato during 2017–2018 were investigated to identify predatory mites that might be useful for the biological control of the phytophagous mites. Three phytophagous and nine predatory mite species were surveyed. The two spotted spider mite Tetranychus urticae Koch of the family Tetranychidae was the dominant pest on these vegetables, while phytoseiids Phytoseiulus persimilis (Athias- Henriot), Typhlodromips swirskii (Athias- Henriot) and Euseius scutalis Chant were the dominant predators. The population of the native or indigenous phytoseiid mite fauna in Egypt such as Phytoseiulus persimilis could be considered as a good biocontrol agent and a part of the Integrated Pest Management (IPM) program in the future. Mite fauna of Egypt especially local populations of Phytoseiulus persimilis can be considered for implementation in future Integrated Pest Management (IPM).     

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.     

Comparison of thread-cutting behavior in three specialist predatory mites to cope with complex webs of <Emphasis Type="Italic">Tetranychus</Emphasis> spider mites

Anti-predator defenses provided by complex webs of Tetranychus mites can severely impede the performance of generalist predatory mites, whereas this may not be true for specialist predatory mites. Although some specialist predatory mites have developed morphological protection to reduce the adverse effects of complex webs, little is known about their behavioral abilities to cope with the webs. In this study, we compared thread-cutting behavior of three specialist predatory mites, Phytoseiulus persimilis, Neoseiulus womersleyi and N. californicus, exhibited inside the complex web of T. urticae. No major difference was observed among them in the basic pattern of this behavior, using chelicerae and palps, and in the number of silken threads severed while moving inside the web. These results and observations suggest that each predator species cut many sticky silken threads to move inside the complex web without suffering from serious obstruction. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Interactions in a tritrophic acarine predator-prey metapopulation system V: Within-plant dynamics of Phytoseiulus persimilis and Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae)

To investigate the relative contributions of bottom-up (plant condition) and top-down (predatory mites) factors on the dynamics of the two-spotted spider mite (Tetranychus urticae), a series of experiments were conducted in which spider mites and predatory mites were released on bean plants. Plants inoculated with 2, 4, 8, 16, and 32 adult female T. urticae were either left untreated or were inoculated with 3 or 5 adult female predators (Phytoseiulus persimilis) one week after the introduction of spider mites. Plant area, densities of T. urticae and P. persimilis, and plant injury were assessed by weekly sampling. Data were analysed by a combination of statistical methods and a tri-trophic mechanistic simulation model partly parameterised from the current experiments and partly from previous data. The results showed a clear effect of predators on the density of spider mites and on the plant injury they cause. Plant injury increased with the initial number of spider mites and decreased with the initial number of predators. Extinction of T. urticae, followed by extinction of P. persimilis, was the most likely outcome for most initial combinations of prey and predators. Eggs constituted a relatively smaller part of the prey population as plant injury increased and of the predator population as prey density decreased. We did not find statistical evidence of P. persimilis having preference for feeding on T. urticae eggs. The simulation model demonstrated that bottom-up and top-down factors interact synergistically to reduce the density of spider mites. This may have important implications for biological control of spider mites by means of predatory mites.     

Correlation between Olfactory Responses, Dispersal Tendencies, and Life-history Traits of the Predatory Mite Neoseiulus Womersleyi (Acari: Phytoseiidae) of Eight Local Populations

To investigate the relationship between foraging behavior and life-history traits of the predatory mite Neoseiulus womersleyi, the olfactory responses, dispersal ratios from a prey patch, predation rates, fecundity, and developmental times in eight local populations of N. womersleyi were investigated. Significant differences among local populations were found in all these traits except fecundity. None of the life-history traits correlated with foraging behavior. A significant positive correlation was found only between the olfactory response and the dispersal ratio. These results suggested that predatory mites with low olfactory responses would stay in a prey patch longer than predatory mites with high olfactory responses.     

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.     

Leaf trichomes influence predatory mite densities through dispersal behavior

Habitat complexity can mediate interactions among predators and herbivores and influences arthropod population density and community structure. The abundance of many predatory mites (Acari: Phytoseiidae) is positively associated with abundance of non‐glandular trichomes. We hypothesized that (1) increasing the complexity (trichome density mimicked with cotton fiber patches) of the habitat that predatory mites encounter on leaves would reduce adult dispersal from plants, and (2) increasing habitat complexity would reduce the time that mites spend walking. Typhlodromus pyri Scheuten retention on plants increased linearly in the presence of trichome mimics; mites placed on plants lacking leaf trichomes showed a behavioral response that led to active dispersal. Phytoseiid retention increased with both fiber patch size and fiber density within patches. Moving fiber patches from the underside of the leaf to the upper leaf surface did not change phytoseiid retention but did alter egg distribution, suggesting trichomes do not exclusively influence phytoseiid behavior. Phytoseiid activity level as measured by the amount of time spent walking did not decrease with the addition of fibers. Overall, increasing habitat complexity in the form of non‐glandular trichomes strongly reduced T. pyri dispersal behavior; the predatory mites showed a consistent preference for complex trichome‐rich habitat that was manifest both rapidly and in absence of predators. Hence, the frequently observed pattern of population‐level accumulation of phytoseiids on trichome‐rich plants appears to be driven by a behavioral response to the presence and abundance of non‐glandular trichomes on the leaf surface manifested in the level of dispersal and/or retention. The primary implication of phytoseiid–habitat interactions for biocontrol programs is that where plants have no trichomes, T. pyri will not establish. Whether this behavioral response pattern is a general response of phytoseiids to leaf trichomes or varies with species is a question that remains unanswered.     

Risk assessment of an exotic biocontrol agent: Phytoseiulus persimilis (Acari: Phytoseiidae) does not establish in rainforest in southeast Queensland

Abstract The Chilean predatory mite, Phytoseiulus persimilis Athias-Henriot, appeared in Australia in 1978 soon after being introduced into New Zealand as a specialized biological control agent of spider mites. It is known to be naturalized in agricultural habitats in southeast Queensland, Australia, although nothing is known about its distribution in native ecosystems. In order to determine whether P. persimilis is able to invade subtropical rainforest, we placed potted bean plants infested with its preferred prey, the two-spotted mite (Tetranychus urticae C.L. Koch), at 50 m intervals for 200 m on either side of the rainforest-field ecotone at four sites in southeast Queensland. Two, 4 and 6 weeks after placement, five leaves were sampled from each pot and any phytoseiid mites present were identified. The initial experiment took place in the spring and was repeated in summer and in autumn of 1997. At all four sites and in all three seasons P. persimilis rapidly colonized all of the pots in fields. In the rainforest, however, some pots were never colonized and significant populations of the predator developed only in the summer, and then only at the first stations, 50 m into the forest. These results suggest that even when its preferred prey is present, subtropical rainforest is not an appropriate habitat for P. persimilis. In addition, we reviewed extensive collections of phytoseiid mites from native forests and synanthropic habitats in Australia and found P. persimilis records only from fields, glasshouses, gardens, weeds, roadsides and similar disturbed habitats dominated by introduced plants, again suggesting that this biocontrol agent is not a rainforest invader.     

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.     

Interactions of two natural enemies of Tetranychus urticae,the fungal entomopathogen Beauveria bassiana and the predatory mite,Phytoseiulus persimilis

The effect of either untreated or treated adults of the spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) by Beauveria bassiana (Bals.) Vuillemin (Ascomycota: Hypocreales) DEBI008 at 1×10⁶ (conidia/ml) was investigated on developmental stages and life table parameters of Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) under laboratory conditions. Four time intervals (0, 24, 48 and 72 h post-inoculation of spider mites) were considered for studying the predator characteristics as different treatments. Duration of each life stage, longevity, reproduction rate, intrinsic rate of natural increase (r _m ), net reproductive rate (R ₀), mean generation time (T) and finite rate of increase (λ) of the P. persimilis were calculated on both untreated and B. bassiana treated spider mite adults. Data analysis showed that longevity and fecundity of predatory mites fed on untreated and treated mites (time interval 0) were higher in comparison with other time intervals after inoculation. The entomopathogenic fungus adversely affected longevity and fecundity of the predatory mite. Fertility life table parameters of predatory mites fed on T. urticae treated by B. bassiana at different time intervals showed that T, R ₀, λ and r _m are strongly affected by the fungus presence and these parameters had significant differences among time treatments. The least r _m value was observed in the time interval of 72 h post-inoculation. The fitness of T. urticae was affected by B. bassiana 24, 48 and 72 h post-inoculation of mite adults, and consequently it caused decreased longevity of P. persimilis and accordingly a decrease in the intrinsic rate of natural increase of the predator.     

Disentangling mite predator‐prey relationships by multiplex PCR

Gut content analysis using molecular techniques can help elucidate predator‐prey relationships in situations in which other methodologies are not feasible, such as in the case of trophic interactions between minute species such as mites. We designed species‐specific primers for a mite community occurring in Spanish citrus orchards comprising two herbivores, the Tetranychidae Tetranychus urticae and Panonychus citri, and six predatory mites belonging to the Phytoseiidae family; these predatory mites are considered to be these herbivores’ main biological control agents. These primers were successfully multiplexed in a single PCR to test the range of predators feeding on each of the two prey species. We estimated prey DNA detectability success over time (DS₅₀), which depended on the predator‐prey combination and ranged from 0.2 to 18 h. These values were further used to weight prey detection in field samples to disentangle the predatory role played by the most abundant predators (i.e. Euseius stipulatus and Phytoseiulus persimilis). The corrected predation value for E. stipulatus was significantly higher than for P. persimilis. However, because this 1.5‐fold difference was less than that observed regarding their sevenfold difference in abundance, we conclude that P. persimilis is the most effective predator in the system; it preyed on tetranychids almost five times more frequently than E. stipulatus did. The present results demonstrate that molecular tools are appropriate to unravel predator‐prey interactions in tiny species such as mites, which include important agricultural pests and their predators.     

First record ofPhytoseiulus persimilis (Acari: Phytoseiidae) in Turkey

The predatory mitePhytoseiulus persimilis Athias-Henriot is widely used for biological control of spider mites in greenhouse. Despite its records from various Mediterranean countries,P. persimilis was not recorded from Turkey. Here we report the natural colonies ofP. persimilis observed along the Mediterranean coast of Turkey.     

Population dynamics of interacting predatory mites,Phytoseiulus persimilis and Neoseiulus californicus,held on detached bean leaves

The success of combined release of the predatory mitesPhytoseiulus persimilis and Neoseiulus californicus insuppression of spider mites may be related to the effects of the interactionsbetween the two predators on their population dynamics. We studied populationgrowth and persistence of the specialist P. persimilis andthe generalist N. californicus reared singly versus rearedin combination after simultaneous and successive predator introductions ondetached bean leaf arenas with abundant prey, Tetranychusurticae, and with diminishing prey. When reared singly with abundantprey, either predator population persisted at high densities to the end of theexperiment. In every predator combination system with abundant prey and variousinitial predator:predator ratios N. californicus displacedP. persimilis. When held singly with diminishing prey, thepopulation of P. persimilis grew initially faster than thepopulation of N. californicus but both species reachedsimilar population peaks. Irrespective whether reared singly or in combination,N. californicus persisted three to five times longer afterprey depletion than did P. persimilis. Regarding thecrucial interactions in the predator combination systems, we conclude thatintraguild predation was a stronger force than food competition and finallyresulted in the displacement of P. persimilis. Previousstudies showed that intraguild predation between the specialist P.persimilis and the generalist N. californicusisstrongly asymmetric favoring the generalist. We discuss the implications ofpotential interactions between P. persimilis andN. californicus to biological control of spider mites.     

Combining predatory mites and film mulching to control Bradysia cellarum (Diptera: Sciaridae) on Chinese chives,Allium tuberosum

The subterranean insect Bradysia cellarum Frey (Diptera: Sciaridae) is a notorious and major pest of Chinese chives, Allium tuberosum Rottler ex Sprengle (Amaryllidaceae) in China. Current chemical control of B. cellarum results in low insecticide efficacy, high cost and pesticide resistance, therefore there is an urgent need for sustainable management. Here, greenhouse experiments were conducted to evaluate the potential biocontrol agent Stratiolaelaps scimitus Womersley (Acari: Laelapidae) against B. cellarum. The number of B. cellarum larvae in soil declined from 17.6 to 0 in 4 months after releasing predatory mites in high density (5,000 adults per row); treatment was less effective under low densities of 2500 adults per row. To determine whether S. scimitus can be used in combination with soil solarization by film mulching over 40 °C for 4 h, we also evaluated heat tolerance of S. scimitus in laboratory and its control efficacy against B. cellarum after high-temperature treatment mimicking the film mulching in greenhouse. As our results showed that egg hatchability of S. scimitus was 2.6% at 38 °C and adult survival rate was 2% at 40 °C for 4 h, respectively, we concluded S. scimitus was largely inviable and could not reproduce at 40 °C. This temperature was the baseline of soil solarization, suggesting predatory mites should be released after soil solarization. When using S. scimitus after soil solarization or when using soil solarization as single treatment, fly larvae declined similarly from initial density of 18 to 0 or 17.2 to 0, respectively, within a month. Thus, our study suggests the potential of S. scimitus as a biocontrol agent of B. cellarum in greenhouse, and the most effective strategy is to combine film mulching and predatory mites (after soil heating) to control B. cellarum in chive productions.

     

Antipredator responses in Tetranychus urticae differ with predator specialization

The behavioural response of Tetranychus urticae to chemical cues from specialist predatory mites, Phytoseiulus persimilis, or generalist predatory bugs, Orius majusculus, on either bean or strawberry was studied in experimental arenas. Predators were placed on the leaf disc for 24 h and removed before T. urticae females were introduced. After 24 h, prey fecundity (number of eggs laid) and dispersal (number of prey drowned in the water barrier) were assessed. Chemical cues from the specialist predator resulted in reduced prey fecundity, significantly different from the generalist predator and control treatments. No interaction effect was found between plant species and prey fecundity, while significantly more eggs were laid on bean than on strawberry. Predator cues irrespective of predator specialization resulted in more prey dispersal than in the control. Findings emphasize the importance of specialization in the predator species complex for the degree and type of antipredator responses and resulting biological control.     

Suitability of different mite prey for the development of the predatory mite,Phytoseiulus persimilis

Development of the phytoseiid mitePhytoseiulus persimilis Athias-Henriot was studied when fed on three mite species as prey. The tenuipalpid mite,Brevipalpus pulcher (Canestrini & Fanzago), is an unsuitable prey forP. persimilis as predatory larvae reared on any stages developed to the protonymphal stage only. WhenP. persimilis larvae were reared on the eriophyid mite,Eriophyes dioscoridis Soliman & Abou-Awad, only a few developed to adulthood, but failed to oviposit. On the contrary, predatory larvae fed on the tetranychid mite,Tetranychus urticae Koch, matured in a significantly shorter period and resulting females exhibited a high rate of reproduction.