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.     

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.     

Preliminary studies of an integrated control programme for cucumber pests and an evaluation of methods of introducing Phytoseiulus persimilis Athias-Henriot for the control of Tetranychus urticae Koch

Preliminary investigations suggest that, when Phytoseiulus persimilis is used to control Tetranychus urticae, the major pest of cucumbers, the control of other pests and powdery mildew can be effected by means of Encarsia formosa for the control of whitefly (Trialeurodes vaporariorum), bed drenches of gamma-BHC for thrips control and dimethirimol for the control of cucumber mildew (Erysiphe cichoracearum). The parasite Aphelinus flavipes failed to control an infestation of Aphis gossypii in one trial. A comparison of different methods of introducing Phytoseiulus confirmed that the best results were obtained when an even, artificial infestation of Tetranychus urticae was established on the crop before the introduction of the predator.     

Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites

We found that intact lima bean plants increased the secretion of extrafloral nectar (EFN) after exposure to Tetranychus urticae-induced plant volatiles. Predatory mites, Phytoseiulus persimilis, dispersed more slowly from an exposed intact plant than from a control plant (plant exposed to volatiles from intact conspecific). The predators also dispersed more slowly from those plants that were provided with extra EFN than from untreated plants. We further show that EFN was a potential alternative food source for P. persimilis. From these results, we concluded that increased EFN was involved in the slow dispersal of P. persimilis from the plants exposed to herbivore-induced plant volatiles. Our data suggest that the increase of EFN in an HIPV-exposed intact plant could be an induced indirect defense against spider mites.     

Olfactory response of Phytoseiulus persimilis (Acari: Phytoseiidae) to untreated and Beauveria bassiana-treated Tetranychus urticae (Acari: Tetranychidae)

Determination of attraction and avoidance behavior of predators is important in concomitant use of multiple natural enemies to control a pest. The olfactory response of the predatory mite Phytoseiulus persimilis was studied to odors related to Tetranychus urticae adults infected by Beauveria bassiana DEBI008 in 0, 24, 48 and 72 h intervals, both in absence and in presence of plants. In plant-present experiments, P. persimilis attraction was neither towards adults of T. urticae infected by 0.02 % Tween 80 (as control), nor to the ones infected by B. bassiana for 0 or 24 h, whereas significant attraction towards the control was observed when tested against T. urticae infected by B. bassiana for 48 or 72 h. In absence of plants, P. persimilis displayed significant avoidance of T. urticae infected by B. bassiana for 48 or 72 h, when their alternative option was 0.02 % Tween 80-infected T. urticae adults. These results indicate that P. persimilis can recognize the presence of B. bassiana and that the predator avoids the fungus. This suggests that the two natural enemy species can be used together in biological control programmes.     

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.     

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.     

Photographic sampling: a photographic sampling method for mites on plants

A photographic sampling method for mites on plants was evaluated using Tetranychus urticae and Phytoseiulus persimilis on pepper plants. It was found to be 92% accurate for T. urticae eggs and 98% accurate for P. persimilis eggs at densities up to 45 eggs per cm² for T. urticae, and up to 3 eggs per cm² for P. persimilis. The motiles of the two species were not confused, nor were they confused with exuviae or other matter.     

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.     

Predation-related odours reduce oviposition in a herbivorous mite

When adult females of the herbivorous mite, Tetranychus urticae, were exposed to the predatory mite, Phytoseiulus persimilis, they laid fewer eggs than females that had not been exposed to P. persimilis when transferred onto a new leaf patch. However, when T. urticae females were exposed to either products of P. persimilis or artificially damaged conspecific eggs on a leaf patch, the number of T. urticae eggs on a new leaf patch did not differ significantly from the control. The reduced oviposition was neither due to the feeding activity on the leaf patch with P. persimilis nor to that on the new leaf patch. There was also no significant difference between the number of T. urticae eggs produced on a new leaf patch following exposure to the odours of a neighbouring leaf patch where there had previously been either P. persimilis or T. urticae adults. However, female T. urticae that had been exposed to odours from neighbouring leaf patches on which both T. urticae and P. persimilis had been placed produced significantly fewer eggs on a new leaf patch than those that had not been exposed to such odours. Neither odours from neighbouring intact leaf patches on which T. urticae eggs were preyed on by P. persimilis, nor odours from a neighbouring Parafilm patch on which T. urticae was preyed on by P. persimilis affected the oviposition of T. urticae. These data suggest that the presence of T. urticae, P. persimilis and a leaf patch are needed for the emission of odours to reduce oviposition in T. urticae.     

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.     

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.     

Integrated pest management of two-spotted mite Tetranychus urticae on greenhouse roses using petroleum spray oil and the predatory mite Phytoseiulus persimilis

From 1995 to 1999, four experiments were conducted on greenhouse roses to assess the effectiveness of the nC24 petroleum spray oil (PSO), D-C-Tron Plus, against two-spotted mite, Tetranychus urticae Koch (Acarina: Tetranychidae), and to determine how the oil could be most efficiently and effectively used in combination with the predatory mite Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae) in an integrated pest management program. The results showed that 0.5% PSO applied fortnightly to roses gave excellent protection from T. urticae infestation when the mite population was not already established. However, PSO applied after roses were infested with T. urticae above the economic threshold only stabilised populations without reducing them below that threshold. Populations of P. persimilis in the upper and lower canopies were unchanged after two sprays of PSO at 7-day intervals, and application of PSO to the upper canopy was as effective in controlling T. urticae in the presence of P. persimilis as spraying the entire plant. Combining PSO with P. persimilis gave better control of T. urticae than using P. persimilis alone. The most cost-effective use of PSO in the presence of P. persimilis is, therefore, to apply spray only to the upper canopy. This will not affect control of powdery mildew with PSO. Comparison of a control program for T. urticae based on the monitored use of synthetic miticides with that based on calendar application of PSO revealed that both gave equally effective control. The benefits of combining PSO and P. persimilis in an integrated pest management program for T. urticae on roses over a program based on synthetic fungicides are discussed.     

Effects of <Emphasis Type="Italic">Euseius stipulatus</Emphasis> on establishment and efficacy in spider mite suppression of <Emphasis Type="Italic">Neoseiulus californicus</Emphasis> and <Emphasis Type="Italic">Phytoseiulus persimilis</Emphasis> in clementine

The two-spotted spider mite, Tetranychus urticae, is one of the most problematic phytophagous pests in Spanish clementine orchards. The most abundant predatory mites in this ecosystem are Euseius stipulatus, Phytoseiulus persimilis and Neoseiulus californicus. Euseius stipulatus is dominant but poorly adapted to utilize T. urticae as prey. It mainly persists on pollen and citrus red mite, Panonychus citri. A recent study suggested that the more efficacious T. urticae predators P. persimilis and N. californicus are negatively affected by lethal and non-lethal intraguild interactions with E. stipulatus. Here, we investigated the potential of N. californicus and P. persimilis to colonize and thrive on young clementine trees infested by T. urticae in presence and absence of E. stipulatus. Presence of E. stipulatus interfered with establishment and abundance of P. persimilis and negatively affected the efficacy of N. californicus in T. urticae suppression. In contrast, the abundance of E. stipulatus was not affected by introduction of a second predator. Trait-mediated effects of E. stipulatus changing P. persimilis and N. californicus behavior and/or life history were the most likely explanations for these outcomes. We conclude that superiority of E. stipulatus in intraguild interactions may indeed contribute to the currently observed predator species composition and abundance, rendering natural control of T. urticae in Spanish clementine orchards unsatisfactory. Nonetheless, stronger reduction of T. urticae and/or plant damage in the predator combination treatments as compared to E. stipulatus alone indicates the possibility to improve T. urticae control via repeated releases of N. californicus and/or P. persimilis.     

Efficacy of <Emphasis Type="Italic">Neoseiulus californicus</Emphasis> and <Emphasis Type="Italic">Phytoseiulus persimilis</Emphasis> in suppression of <Emphasis Type="Italic">Tetranychus urticae</Emphasis> in young clementine plants

Tetranychus urticae is one of the most damaging tetranychid mites affecting clementine orchards in Spain, where natural control is insufficient. Furthermore, in clementine nurseries, tender foliage is highly susceptible to attack and natural enemies are almost always absent. Therefore, acaricides are often used indiscriminately. Alternative control measures are necessary, both in commercial orchards and clementine nurseries. In order to assess the efficacy of inoculative releases of N. californicus and P. persimilis to reduce T. urticae populations in young Spanish clementine plants, a semi-field experiment was conducted and repeated in three seasons (spring, summer and autumn). Phytoseiulus persimilis was highly effective in reducing both T. urticae infestations and the damage level inflicted on plants at both release rates evaluated (40 and 80 phytoseiids/plant) and all three periods considered. By contrast, N. californicus demonstrated low performance under certain conditions. The results of this study could be adapted and transferred to nurseries and young citrus plantations.     

Plant architecture and prey distribution influence foraging behavior of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae)

The arrangement, number, and size of plant parts may influence predator foraging behavior, either directly, by altering the rate or pattern of predator movement, or, indirectly, by affecting the distribution and abundance of prey. We report on the effects of both plant architecture and prey distribution on foraging by the predatory mite, Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae), on cucumber (Cucumis sativus L.). Plants differed in leaf number (2- or 6-leafed), and there were associated differences in leaf size, plant height, and relative proportions of plant parts; but all had the same total surface area. The prey, the twospotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae), were distributed either on the basal leaf or on all leaves. The effect of plant architecture on predator foraging behavior varied depending on prey distribution. The dimensions of individual plant parts affected time allocated to moving and feeding, but they did not appear to influence the frequency with which predators moved among different plant parts. Overall, P. persimilis moved less, and fed upon prey longer, on 6-leafed plants with prey on all leaves than on plants representing other treatment combinations. Our findings suggest that both plant architecture and pattern of prey distribution should be considered, along with other factors such as herbivore-induced plant volatiles, in augmentative biological control programs.     

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.     

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.     

Pre-adult development of Phytoseiulus persimilis on diets of Tetranychus urticae and Tetranychus lintearius: implications for the biological control of Ulex europaeus

Predation by the phytoseiid mite, Phytoseiulus persimilis, is considered a major threat to the effectiveness of biological control of gorse, Ulex europaeus, using Tetranychus lintearius. To assess this threat and to determine if the impact of P. persimilis on T. lintearius populations is comparable to its impact on T. urticae populations, its development and predator : prey generation time ratios were assessed. The pre-adult mortality and development time of two populations of P. persimilis fed on two diets, T. urticae and T. lintearius, were determined at two temperatures, 14 and 24°C. There were no significant differences in either mortality or development time between the two populations of P. persimilis at these temperatures. There is therefore no evidence that the two tested populations of P. persimilis are behaving as different strains. Similarly, diet had no significant effect on either mortality or development time at these temperatures. At 14°C the mortality of P. persimilis was significantly higher and development was significantly longer than at 24°C. Using pre-adult development as a surrogate for generation times, predator : prey generation time ratios were calculated between P. persimilis and both T. urticae and T. lintearius using data from this and other studies. The predator : prey generation time ratios between P. persimilis and T. lintearius were lower than those between P. persimilis and T. urticae. These results indicate that the impact of P. persimilis on T. lintearius populations is likely to be comparable to its impact on T. urticae populations. This provides further evidence that predation by P. persimilis is having a deleterious effect on T. lintearius populations and therefore reducing its effectiveness as a biological control agent for gorse.