Innate responses of the predatory mite <Emphasis Type="Italic">Phytoseiulus persimilis</Emphasis> to a herbivore-induced plant volatile

The responses of the predatory mite P. persimilis to herbivore-induced plant volatiles are at least partly genetically determined. Thus, there is potential for the evolution of this behaviour by natural selection. We tested whether distinct predator genotypes with contrasting responses to a specific herbivore-induced plant volatile, i.e. methyl salicylate (MeSa), could be found in a base population collected in the field (Sicily). To this end, we imposed purifying selection on individuals within iso-female lines of P. persimilis such that the lines were propagated only via the individual that showed either a preference or avoidance of MeSa. The responses of the lines were characterized as the mean proportion of individuals choosing MeSa when given a choice between MeSa and clean air. Significant variation in predator responses was detected among iso-female lines, thus confirming the presence of a genetic component for this behaviour. Nevertheless, we did not find a significant difference in the response to MeSa between the lines that were selected to avoid MeSa and the lines selected to prefer MeSa. Instead, in the course of selection the lines selected to avoid MeSa shifted their mean response towards a preference for MeSa. An inverse, albeit weaker, shift was detected for the lines selected to prefer MeSa. We discuss the factors that may have caused the apparent lack of a response to selection within iso-female line in this study and propose experimental approaches that address them.     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

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.     

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.     

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.     

A method to assess the effects of pesticides on the predatory mite Phytoseiulus persimilis (Acari Phytoseiidae) in the laboratory

Phytoseiulus persimilis Athias-Henriot (Acari Phytoseiidae) is a major predator of Tetranychus urticae (Acari Tetranychidae). The performance of P. persimilis in controlling T. urticae may be altered by pesticides used to manage other pests. Therefore, knowledge of the side-effects of pesticides is essential for IPM. A number of laboratory methods were suggested to evaluate pesticide side-effects on predatory mites. Most methods assess residual effects only, and a number of them are characterised by high predator escape rates from experimental units. A method aimed at evaluating the topical and residual effects of pesticides on P. persimilis is herein described. Mites were treated by microimmersion and then reared in holding cells, on bean leaves previously dipped in a pesticide solution. Three insecticides (pyrethrins, spinosad and thiamethoxam), an insecticide-acaricide (abamectin), and two fungicides (azoxystrobin and tolylfluanide) were evaluated. The strain of P. persimilis used for evaluation was collected from unsprayed vegetable plants. All the pesticides affected the survival and fecundity of P. persimilis. Pesticides did not affect the egg-hatching of P. persimilis females exposed to pesticides. Pyrethrins and abamectin proved to be more toxic than other pesticides, and thiamethoxam was more toxic than spinosad, azoxystrobin and tolylfluanide. The escape rate from experimental units was lower than 5% in all trials. Additional experiments were performed on P. persimilis eggs by dipping leaves with eggs in the pesticide solution. None of the pesticides affected egg survival. Semi-field trials conducted on potted bean plants obtained results similar to those reported in laboratory trials.     

Phenotypic plasticity in anti-intraguild predator strategies: mite larvae adjust their behaviours according to vulnerability and predation risk

Interspecific threat-sensitivity allows prey to maximize the net benefit of antipredator strategies by adjusting the type and intensity of their response to the level of predation risk. This is well documented for classical prey-predator interactions but less so for intraguild predation (IGP). We examined threat-sensitivity in antipredator behaviour of larvae in a predatory mite guild sharing spider mites as prey. The guild consisted of the highly vulnerable intraguild (IG) prey and weak IG predator Phytoseiulus persimilis, the moderately vulnerable IG prey and moderate IG predator Neoseiulus californicus and the little vulnerable IG prey and strong IG predator Amblyseius andersoni. We videotaped the behaviour of the IG prey larvae of the three species in presence of either a low- or a high-risk IG predator female or predator absence and analysed time, distance, path shape and interaction parameters of predators and prey. The least vulnerable IG prey A. andersoni was insensitive to differing IGP risks but the moderately vulnerable IG prey N. californicus and the highly vulnerable IG prey P. persimilis responded in a threat-sensitive manner. Predator presence triggered threat-sensitive behavioural changes in one out of ten measured traits in N. californicus larvae but in four traits in P. persimilis larvae. Low-risk IG predator presence induced a typical escape response in P. persimilis larvae, whereas they reduced their activity in the high-risk IG predator presence. We argue that interspecific threat-sensitivity may promote co-existence of IG predators and IG prey and should be common in predator guilds with long co-evolutionary history.     

Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey‐related cues

Most terrestrial plants are associated with arbuscular mycorrhizal fungi but research on the effects of arbuscular mycorrhizal symbiosis on aboveground plant‐associated organisms is scarcely expanded to tri‐trophic systems. The arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. enhances fitness of the two‐spotted spider mite Tetranychus urticae Koch and its natural enemy, the predatory mite Phytoseiulus persimilis Athias‐Henriot, via changes in host plant and prey quality, respectively. In the present study, it is hypothesized that gravid P. persimilis are able to recognize arbuscular mycorrhiza‐enhanced prey quality and behave accordingly. In two experiments, on leaf arenas and in cages, P. persimilis is given a choice between prey patches deriving from mycorrhizal and non‐mycorrhizal bean plants (Phaseolus vulgaris L.) as feeding and oviposition sites. The use of cages allows the manipulation of distinct patch components acting as possible cues to guide predator foraging and oviposition behaviours, such as eggs produced and traces (webbing and faeces) left by the spider mite females. Both experiments show that P. persimilis preferentially resides close to prey fed on mycorrhizal plants. The cage experiment reveals that P. persimilis uses direct prey‐related cues, mainly derived from eggs, to discern prey quality and preferentially oviposits close to prey from mycorrhizal plants. This is the first study to document that predators recognize arbuscular mycorrhiza‐induced changes in herbivorous prey quality via direct prey‐related cues.     

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.     

Plant spatial distribution and predator–prey ratio affect biological control of the twospotted spider mite Tetranychus urticae (Acari: Tetranychidae) by the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae)

A greenhouse experiment was conducted to determine the effect of plant spacing and predator–prey ratio on dispersal and foraging efficiency of the predatory mite, Phytoseiulus persimilis, on the twospotted spider mite, Tetranychus urticae. When predators were released at the end of spider mite-infested arrays of lima bean plants that had either no spacing or two different patterns of spacing among plant rows, plant damage was uniformly low throughout the experiment at both predator–prey ratios (1:10 and 3:10) in the treatment with no spacing. In contrast, damage was higher in both treatments where plant rows were interrupted by spacing. At the 1:10 ratio, more plants closer to the predator release point experienced moderate damage than at the 3:10 ratio where only the plant rows farthest from the release point had unacceptable damage. Our findings suggest that point releases of P. persimilis at the standard 1:10 predator–prey ratio should be effective within a diameter of at least 65?cm on mite-infested patches of plants where pots are touching. However, if gaps in plant rows exist, even large numbers of predators may not be sufficient to protect parts of the crop unless predators are released at shorter fixed points in the greenhouse crop.     

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.     

Changes in body weight of two species of predatory mites (Acarina: Phytoseiidae) as a consequence of feeding in an interactive system

Changes in body weight of two species of predatory mites,Phytoseiulus persimilis Athias-Henriot andAmblyseius degenerans (Berlese), when each species was feeding alone on the prey miteTetranychus pacificus McGregor, were determined in the laboratory. The body weight of a starved adult femaleP. persimilis could increase 105.6% (13.05 g) to full satiation, whereasA. degenerans increased 43.2% (7.6 g). A simple model is used to describe the weight changes of each species. Changes in body weight also were determined when each of the two species fed with conspecifics at a high and low predator density. WithP. persimilis there was a reduction in body weight as well as in reproduction and in the number of prey killed when feeding at a high density of conspecifics. These reductions were not observed withA. degenerans. WhenP. persimilis fed with heterospecifics (A. degenerans), reductions in these three variables were less marked. The reductions are attributed primarily to the effect of sharing prey meals with conspecifics. Possible mechanisms for these reductions through meal-sharing are discussed.     

The feeding behaviour of Phytoseiulus persimilis (Acarina: Phytoseiidae), particularly as affected by certain pesticides

Detailed observations were made of the behaviour of Phytoseiulus persimilis while searching for, identifying and feeding on eggs of Tetranychus urticae. A theory is proposed to explain how P. persimilis may identify prey eggs and distinguish them from non-prey objects. The existence of a water-soluble feeding stimulant on prey eggs is postulated. The effect of residues of captan, dinocap and malathion on the feeding behaviour of P. persimilis was investigated. Residues of the fungicide dinocap on the eggs of the prey did not affect acceptance by the predator, but captan had a marked repellent effect. Malathion had an even stronger repellent effect. It is suggested that, by making the prey eggs less acceptable to the predator, the use of certain fungicides could render more difficult the prediction of population interactions on which biological control depends. We wish to thank Dr N. W. Hussey of the Glasshouse Crops Research Institute for helpful comments and for supplying predatory mites. Mr Jackson wishes to thank the Overseas Development Administration for financial support during this work.     

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.     

Optimum release times for biological control of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) by Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae) on the strawberry in greenhouses

The effectiveness of the predatory mite Phytoseiulus persimilis Athias‐Henriot (Acari: Phytoseidae) in controlling the two‐spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) was evaluated in commercial strawberry greenhouses in two areas of Korea. Optimum release times for P. persimilis were investigated by case studies. Control effects of the two‐spotted spider mite by release of the predatory mite were shown. There was mostly good control by the release of P. persimilis when there were fewer than 0.9 T. urticae per leaf. We recommend it would be ideal to release P. persimilis twice in December and once in February for very early strawberry harvest, and three times from February to March (after overwintering) for early harvest.     

Potential long-term storage of the predatory mite <Emphasis Type="Italic">Phytoseiulus</Emphasis><Emphasis Type="Italic">persimilis</Emphasis>

Increasing the ability to store mass-reared natural enemies during periods or seasons of low demand is a critical need of the biocontrol industry. We tested the hypothesis that chemicals can enhance long-term cold storage of a predatory mite Phytoseiulus persimilis Athias-Henriot. The research objective was to determine the effect of cryoprotectant and carbohydrate chemicals on in-storage survival of predators. In-storage survival at 8°C was greater for predators sprayed with glycerol (5%, v/v) or glucose (10% and 20%, v/v) than with water spray controls. After 74 days in the cryoprotectant experiment, predator survival declined to 11.5% in the 5% glycerol treatment and 7.8% in the water spray control. After 88 days in the carbohydrate experiment, predator survival declined to 22% in the 20% glucose treatment and 2% in the water spray control. Although many individuals expired within 50 days in both experiments, a few females survived more than 200 days. This research suggests that select cryoprotectants and carbohydrates have a limited capacity to facilitate long-term storage of P. persimilis.     

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.     

Canalization of body size matters for lifetime reproductive success of male predatory mites (Acari: Phytoseiidae)

The adaptive canalization hypothesis predicts that highly fitness‐relevant traits are canalized via past selection, resulting in low phenotypic plasticity and high robustness to environmental stress. Accordingly, we hypothesized that the level of phenotypic plasticity of male body size of the predatory mites Phytoseiulus persimilis (low plasticity) and Neoseiulus californicus (high plasticity) reflects the effects of body size variation on fitness, especially male lifetime reproductive success (LRS). We first generated small and standard‐sized males of P. persimilis and N. californicus by rearing them to adulthood under limited and ample prey supply, respectively. Then, adult small and standard‐sized males were provided with surplus virgin females throughout life to assess their mating and reproductive traits. Small male body size did not affect male longevity or the number of fertilized females but reduced male LRS of P. persimilis but not N. californicus. Proximately, the lower LRS of small than standard‐sized P. persimilis males correlated with shorter mating durations, probably decreasing the amount of transferred sperm. Ultimately, we suggest that male body size is more strongly canalized in P. persimilis than N. californicus because deviation from standard body size has larger detrimental fitness effects in P. persimilis than N. californicus. © 2014 The Authors. Biological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 889–899.     

Airborne dispersal ofPhytoseiulus persimilis (Acarina:Phtyoseiidae) from a raspberry garden in New Zealand

Airborne dispersal of the predatory mitePhytoseiulus persimilis Athias-Henriot and its preyTetranychus urticae Koch was recorded by trapping mites in silicon grease on microscope slides mounted on a cross-shaped frame placed horizontally 2.5 m above ground level (0.5 m above the top of the crop). Both species were also recorded on raspberry foliage, and population changes there were closely mirrored by numbers caught in the trap.Phytoseiulus persimilis was trapped on slides and recovered from foliage until leaf fall which occurred 6 weeks after the last prey was found. The decline in predator numbers on the foliage closely followed the decline in prey numbers, but the decline of predators on the aerial trap more closely mirrored the decline in the proportion of sample leaves with predators.     

Development of biological methods for the control of Tetranychus urticae on tomatoes using Phytoseiulus persimilis

The biological control of red spider mite using the predatory mite Phytoseiulus persimilis was investigated in 1971, 1972 and 1974. Experiments in small glasshouse compartments showed that the predator should be introduced when the leaf damage index is < 0–3. Uniform and/or patch introductions of P. persimilis at different rates were made into naturally occurring red spider mite infestations on commercial nurseries. In eleven of the seventeen experiments good control was achieved. Introduction of the predator soon after damage appeared on the crop was essential. Poor control was obtained when the predator failed to establish itself, where very large numbers of diapausing mites emerged and built up rapidly or where the predator, introduced into patches, failed to colonize infested plants elsewhere in the crop. When spider mites and predators were introduced on to one-fifth or one-tenth of the plants in a propagating house, a satisfactory interaction was maintained for 4–6 wk after planting out. The predators then died unless red spider mites emerged from diapause or were introduced. Petroleum oil sprays were sometimes used successfully in the presence of the predator to reduce high red spider mite infestations and re-establish the biological equilibrium.