Searching behavior and associational response ofZetzellia mali (Acarina: Stigmaeidae)

Experimental tests of the hypothesis that natural selection favors predators that search and select prey species that are more profitable are reported. The predator studies was the stigmaeid mite,Zetzellia mali (Ewing). It was observed thatAculus schlechtendali (Nalepa) andPanonychus ulmi (Koch) were more profitable prey thanTetranychus urticae Koch. However,Z. mali attacks prey independently of their nutritional value. Behavioral observations and experiments documented thatZ. mali does not detect kairomones of the prey species. Therefore, prey location is due only to random encounters. Apparently,Z. mali does not search and select prey that are more profitable. The correlation coefficients ofZ. mali, A. schlechtendali, andP. ulmi were investigated in an apple tree. Results revealed that the association depends on season and type of prey.Zetzellia mali andA. schlechtendali were positively associated in the spring (r=0.3,P<0.05) and fall (r=0.36,P<0.01).Zetzellia mali andP. ulmi were not statistically associated. The term associational response is proposed as an ecological process that quantifies the association of predator and prey. The associational-response data suggest thatZ. mali, in the natural ecosystem, responds more to the density ofA. schlechtendali than to the density ofP. ulmi.     

Assessment of Amblyseius fallacis (Acari: Phytoseiidae) for biological control of tetranychid mites in an Ontario peach orchard

We introduced a mass-reared pyrethroid-resistant strain of the predatory phytoseiid mite Amblyseius fallacis (Garman) into an Ontario peach orchard in an attempt to control populations of the phytophagous mites Panonychus ulmi Koch and Tetranychus urticae Koch (Acari: Tetranychidae). Releases of 1,000 and 2,000 mites per tree were made, at three different times. The release of 2,000 mites per tree in June and in July resulted in significantly higher phytoseiid densities than was observed on control trees. However, densities of P. ulmi or T. urticae were not significantly affected by any release rate or by timing. The release of 1,000 A. fallacis per tree, or of any density in August, did not significantly increase phytoseiid abundance. In the following year, population dynamics of both phytoseiid and phytophagous mites were not significantly affected by the previous year's release. Amblyseius fallacis can be a useful predator in some fruit orchards. However, further research is necessary into the timing and rate of release, modified spray programmes, and with different crops, in order to clarify the role of this species for biological control in Ontario peach orchards.     

Some effects of pre-release host-plant on the biological control of Panonychus ulmi by the predatory mite Amblyseius fallacis

Amblyseius fallacis Garman has been selected for pyrethroid resistance and mass reared for experimental release as a biological control agent for tetranychid mites on a number of crops in Canada. Several releases of this predator onto apple and peach trees have failed to result in the establishment of A. fallacis, or in the biological control of Panonychus ulmi Koch. Here, we test the hypothesis that the change of host-plant at the time of release is a critical factor in the establishment of A. fallacis for biological control of P. ulmi. Functional and numerical response studies were undertaken on two populations of A. fallacis: a wild strain collected from the canopy foliage of an apple orchard near Vineland, Ontario; and a second strain reared on bean plants in a commercial insectary with Tetranychus urticae as prey. Each population consumed significantly more P. ulmi and produced significantly more eggs when on leaf disks from the plant species they were reared on, than on leaf disks from the novel host plant. A further experiment was conducted to determine if establishment and biological control of mass-reared A. fallacis could be affected by rearing a population for a short term on apple leaves prior to release on apple trees. Three release treatments were made into potted apple trees in a glasshouse, using predators commercially mass-reared on bean and T. urticae: A. fallacis released directly; A. fallacis reared in the laboratory for four weeks on bean and T. urticae; A. fallacis reared on apple leaves and T. urticae for four weeks. They were compared with a control treatment lacking predator release. Contrary to results of the functional and numerical response studies, no difference was observed between release treatments. All release treatments adding A. fallacis resulted in a similar, if limited, degree of biological control of P. ulmi. These results indicated that there may be short-term effects of host plant on the establishment of A. fallacis and biological control of P. ulmi, which in our study were observed as an initial reduction of the predatory response. However, in a test, the predators appeared to overcome these short-term effects and successfully established on the new host-plant to control P. ulmi.     

Prey preference of the phytoseiid miteTyphlodromus pyri 1. Response to volatile kairomones

Using a Y-tube olfactometer, a study has been made of the response of females of the predatory miteTyphlodromus pyri Scheuten (Acarina: Phytoseiidae) to volatile kairomones of three prey species: the European red spider mite (Panonychus ulmi (Koch)), the two-spotted spider mite (Tetranychus urticae Koch) and the apple rust mite (Aculus schlechtendali (Nalepa)).Predators that had been reared onT. urticae responded only to the volatile kairomone ofP. ulmi. In contrast, when reared onVicia faba L. pollen, they responded to the kairomones of all three prey species. Pollen-reared predators, offered a choice between kairomones of two different prey species, prefer theP. ulmi kairomone to those ofA. schlechtendali orT. urticae.The difference in response between predators reared onV. faba pollen andT. urticae seems to be caused by the low carotenoid content ofV. faba pollen. Predators that had been reared onV. faba pollen mixed with crystalline -carotene behaved in a way similar to conspecific that had been reared on the carotenoid-rich prey miteT. urticae. Obviously, pollen-rearedT. pyri females are in need of carotenoids, which can be obtained from, e.g.,P. ulmi, T. urticae orA. schlechtendali. This may explain why pollen-reared predators respond to more prey species thanT. urticae-reared predators.WhyT. pyri females need carotenoids has not been established. The only known function of carotenoids in mites is involvement in diapause induction. However, as pollen-rearedT. pyri enter reproductive diapause under short-day conditions, they either extract sufficient amounts of carotenoids fromV. faba pollen, or do not need carotenoids for diapause induction.Apart from the effect of dietary requirements on prey selection, food deprivation also affects the predator's response to kairomones. All the data mentioned above have been obtained for predators that had been starved for 20 h. Predators that had been reared onT. urticae and starved for 48 h before the experiment did respond to the volatile kairomone ofT. urticae in contrast to predators from the same culture that had been starved for 20 h. Thus foraging decisions byT. pyri are affected by both starvation time and specific hunger for carotenoids.     

Factors affecting biological control of apple mites by mixed populations ofMetaseiulus occidentalis andTyphlodromus pyri

Metaseiulus occidentalis (Nesbitt) andTyphlodromus pyri Scheuten have complementary features/ traits that enable them to control effectively plant-feeding mites on apple. Populations of both predators gave as good or better biological control of the apple rust mite (Aculus schlechtendali Nalepa), European red mite (Panonychus ulmi Koch) and two-spotted spider mite (Tetranychus urticae (Koch)) than single-predator populations. With mixed predators,M. occidentalis provided better control of spider mites the first season after release, butT. pyri gave better control in the second season. Several factors affected the ability of predators to provide biological control: When prey were dense,M. occidentalis rapidly increased during the warm mid-summer, whileT. pyri provided greater predation when it was cool at the start or end of the growing season. When few prey were present, searching byM. occidentalis was more confined on individual apple leaves, but it migrated between leaves and trees more often. Pollen feeding, cannibalism and interspecific predation were more common byT. pyri. In fall, oviposition byM. occidentalis stopped sooner and in the following spring,T. pyri reproduced beforeM. occidentalis. Research needs and management of mixed-predator populations are discussed.     

Feeding preference of Zetzellia mali: does absolute or relative abundance of prey matter more?

The importance of the acarine predator, Zetzellia mali, in the control of phytophagous mites in apple orchards is not well understood. Zetzellia mali tends to prefer the eriophyid, Aculus schlechtendali, over the economically more significant tetranychid, Panonychus ulmi, but quite a wide range of preference values have been reported in the literature. In sets of laboratory choice trials, we determined that prey preference of this predator varies with the relative but not absolute density of its prey. We attempt to explain these results in terms of behavioural mechanisms and discuss the potential implications of our results for the effectiveness of Z. mali in the biological control of phytophagous mites in apple orchards.     

Factors influencing the acaricidal activity of flucycloxuron

Contact activities of flucycloxuron on immature stages of the two-spotted spider mite (Tetranychus urticae (Koch)) and the European red mite (Panonychus ulmi (Koch)) gradually decrease in the successive developmental stages. The levels of contact activity of flucycloxuron on larvae and protonymphs ofT. urticae andP. ulmi are of the same order. Deutonymphs ofT. urticae are less susceptible to contact activity than the similar stage ofP. ulmi. In adultT. urticae, the transovarial ovicidal activity was used as an indicator for cuticular penetration. More than 90% of the maximal penetration into adult mites occurs within 8 h. Reversibility of the transovarial activity was not observed after 24 h, but did occur after a subsequent 48 h stay on untreated leaves. The ovo-larvicidal activity of flucycloxuron onP. ulmi after treatment of apple leaves is strongly negatively influenced by leaf age, partly by lower retention of the spray liquid on the leaves. Leaf penetration was measured by application of flucycloxuron on leaf uppersides and assessment of the transovarial activity in mites (P. ulmi orT. urticae) infested on the undersides, one day after treatment. In this test system, leaf penetration was found to be strongly species dependent. Penetration was high in cucumber, moderate in French beans, cotton, roses and strawberry, but low in apple and pepper. Leaf penetration in French bean plants is drastically reduced at increasing leaf age. The overall positive effect of increase in relative air humidity on leaf penetration, is statistically highly significant (P=0.001) for French beans and almost significant (P=0.08) for cucumbers. WithT. urticae on French bean it was found that in this test flucycloxuron needs more than one day for maximal leaf penetration. Although in apple leaves penetration from uppersides was low, penetration from undersides was much higher. The surfactants Arkopal N 130, Silwet L-77 and X2-5309 enhance penetration from leaf under-sides.     

Analysis of prey preference in phytoseiid mites by using an olfactometer,predation models and electrophoresis

Prey preference of three phytoseiid species,Typhlodromus pyri Scheuten,Amblyseius potentillae (Garman) andA. finlandicus (Oudemans) which occur in Dutch orchards, was analysed with respect to two economically important phytophagous mites, the European red spider mitePanonychus ulmi (Koch), and the apple rust miteAculus schlechtendali (Nalepa). Two types of laboratory experiments were carried out: (1) olfactometer tests to study the response when volatile kairomones of both prey species were offered simultaneously; and (2) predation tests in mixtures of the two prey species and comparison with calculated predation rates, using a model provided with parameters estimated from experiments with each prey species alone. In addition, the diet of field-collected predators was analysed using electrophoresis. For each predator species the results of the different tests were consistent, in thatT. pyri andA. potentillae preferredP. ulmi overA. schlechtendali, whereasA. finlandicus preferredA. schlechtendali overP. ulmi.     

Prey preference of the phytoseiid miteTyphlodromus pyri 2. Electrophoretic diet analysis

The prey selection of the phytoseiid miteTyphlodromus pyri Scheuten was studied by using polyacrylamide gel electrophoresis to analyse the diet of field-collected predators. The predators were obtained from an orchard where the phytophagous prey mitesPanonychus ulmi (Koch) andAculus schlechtendali (Nalepa) were present in various density ratios.Esterases of both prey species were identified in the predators, but on all sampling datesP. ulmi esterases were discovered much more frequently than those ofA. schlechtendali. The data show thatT. pyri hardly fed onA. schlechtendali over a range of prey density ratios. It is therefore concluded thatT. pyri prefersP. ulmi toA. schlechtendali.     

Do phytoseiid mites select the best prey species in terms of reproductive success?

Optimal foraging theory predicts that predators prefer those prey species that are most rewarding in terms of reproductive success, which is dependent on prey quality and prey availability. To investigate which selection pressures may have moulded prey preference in an acarine system consisting of two prey species and three predator species, we tested whether prey preference of the predators is matched by the associated reproductive success.The predators involved areAmblyseius finlandicus (Oudemans),Am. potentillae (Garman) andTyphlodromus pyri Scheuten. The prey species are the apple rust mite (Aculus schlechtendali (Nalepa)) and the fruit-tree red spider mite (Panonychus ulmi (Koch)).Reproductive success was assessed in terms of intrinsic rate of increase and for one predator also in terms of diapause induction. All three predator species reached highest reproductive success on the same prey species: apple rust mite. This was most pronounced for the predatorAm. finlandicus, because its larval stage suffered severe mortality when feeding onP. ulmi.An independent study on prey preference of the three predator species (Dicke et al., 1988) revealed thatAm. finlandicus prefersAc. schlechtendali toP. ulmi, whereas the other two predator species have the reverse preference.Thus, on the basis of current data, prey preference ofAm. finlandicus can be understood in terms of reproductive success. However, this is not so for prey preference ofT. pyri andAm. potentillae. Investigations needed for a better understanding of prey preference of the last-named two predator species are discussed.     

Effects of acaricides,pyrethroids and predator distributions on populations of <Emphasis Type="Italic">Tetranychus urticae</Emphasis> in apple orchards

We sampled mites in three apple orchards in Nova Scotia, Canada, that had been inoculated with pyrethroid-resistant Typhlodromus pyri and had a history of Tetranychus urticae outbreaks. The objective of this study was to monitor populations of T. urticae and phytoseiid predators on the ground and in trees and to track dispersal between the two habitats. Pesticides were the chief cause of differences in mite dynamics between orchards. In two orchards, application of favourably selective acaricides (abamectin, clofentezine) in 2002, coupled with predation by T. pyri in trees and Neoseiulus fallacis in ground cover, decreased high T. urticae counts and suppressed Panonychus ulmi. By 2003 phytoseiids kept the tetranychids at low levels. In a third orchard, application of pyrethroids (cypermethrin, lambda-cyhalothrin), plus an unfavourably selective acaricide (pyridaben) in 2003, suppressed phytoseiids, allowing exponential increases of T. urticae in the ground cover and in tree canopies. By 2004 however, increasing numbers of T. pyri and application of clofentezine strongly reduced densities of T. urticae in tree canopies despite high numbers crawling up from the ground cover. Another influence on T. urticae dynamics was the distribution of the phytoseiids, T. pyri and N. fallacis. When harsh pesticides were avoided, T. pyri were numerous in tree canopies. Conversely, only a few N. fallacis were found there, even when they were present in the ground cover and on tree trunks. Low numbers were sometimes due to pyrethroid applications or to scarcity of prey. Another factor was likely the abundance of T. pyri, which not only competes with N. fallacis, but also feeds on its larvae and nymphs. The scarcity of a specialist predator of spider mites in trees means that control of T. urticae largely depends on T. pyri, a generalist predator that is not particularly effective in regulating T. urticae. The Canadian Crown's right to retain a non-exclusive, royalty-free licence in and to any copyright is acknowledged.     

Control of phytoseiids in a spider mite mass-rearing system (Acari: Phytoseiidae,Tetranychidae)

Phytoseiid mites which contaminated the spider mite colony and interfered with the mass-rearing of spider mites were controlled by dipping in hot water. Immersion for 60 s in water of 50°C killed all stages ofAmblyseius fallacis (Garman),A. womersleyi Schicha andPhytoseiulus persimilis (Athias-Henriot) (Acari: Phytoseiidae). Only approximately 0.3% of theA. womersleyi eggs hatched, and this seems negligible. The populations ofTetranychus kanzawai Kishida andT. urticae (Koch) (Acari: Tetranychidae) were reduced. However, they recovered well. Although this treatment resulted in the withering of some soybean seedlings, the next trifoliate leaf to be produced was normal. A very satisfactory result was obtained when this technique was applied to the mass-rearing system.     

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

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

Effect of the width of the herbicide strip on mite dynamics in apple orchards

Herbicide strips are used in apple orchards to promote tree growth and survival, to increase yield and to reduce the risk of rodent damage to tree bark. However, herbicide strips, particularly wider ones, may cause problems including soil erosion, reduced organic matter, leaching of nitrates into ground water and increased incidence of plant diseases and pests, including two-spotted spider mites, Tetranychus urticae Koch. In this 2 year study we monitored mite dynamics in apple trees and used sticky bands on tree trunks to determine rates of T. urticae immigration into Nova Spy apple trees in plots with wide (2 m) or narrow (0.5 m) herbicide strips. Use of wider herbicide strips promoted two risk factors that could trigger outbreaks of tetranychid mites. First, concentrations of leaf N in apple trees were higher and those of P and K were lower with the wide strips. Such changes in nutritional quality of leaves would increase the potential for more rapid population growth of T. urticae, and to a lesser extent, the European red mite, Panonychus ulmi (Koch). Second, there were higher rates of T. urticae immigration from the ground cover vegetation into the trees. In 2006, and for most of 2007, densities of T. urticae were higher with wide herbicide strips, whereas densities of P. ulmi were not enhanced. However, by late August to early September in 2007, densities of both tetranychids were lower with wide herbicide strips. This is because both risk factors were counterbalanced, and eventually negated, by the enhanced action of phytoseiid predators, mostly Typhlodromus pyri Scheuten. From July through September 2006, ratios of phytoseiids to tetranychids were always several-fold lower with wide herbicide strips but in 2007, from mid-July onwards, predator–prey ratios were usually several-fold higher with wide strips. However, this numerical response of phytoseiids to prey density can only occur where the pesticide program in orchards is not too harsh on phytoseiids. Hence the impact of width of herbicide strip is contingent on the composition and size of the phytoseiid complex and the impact of pesticides on predation.     

Does prey preference change as a result of prey species being presented together? Analysis of prey selection by the predatory mite Typhlodromus pyri (Acarina: Phytoseiidae)

Summary Prey-selection behaviour of the phytoseiid mite Typhlodromus pyri Scheuten was analysed with a Markovtype model of feeding-state dynamics and feeding-state dependent searching behaviour (Sabelis 1981, 1986, 1989; Metz and Van Batenburg 1985a, b). All behavioural characteristics of the predator which are independent of the feeding state were represented by one parameter. The remaining feeding-state dependent characteristics were represented by a function of the feeding state, with one parameter. The best parameter values to describe a predator-prey interaction were determined by fitting the model to the predation rates in monocultures. Under the assumption that the parameter values are not dependent on the composition of prey species supply, the diet of the predators in mixed cultures was predicted from parameters estimated in monoculture experiments.Two prey types, apple rust mite (Aculus schlechtendali (Nalepa)) adults and European red spider mite (Panonychus ulmi (Koch)) larvae were studied. A large discrepancy was observed between calculated and experimentally determined predation rates of T. pyri in mixed cultures: the predators actually killed 3–7 times more P. ulmi larvae than was predicted by the model.The large difference between observed and predicted predation rates in mixed cultures cannot be explained by changes in the behaviour of the prey species as a result of being together. Therefore, it seems likely that the prey selection behaviour of the predator was different when prey species were presented together than when presented singly. Apparently the predatory mite T. pyri prefers P. ulmi to S. schlechtendali.     

Simulation model of the European red mite andTyphlodromus pyri in New Zealand apple orchards

A deterministic model of the European red mitePanonychus ulmi (Koch) and its predatorTyphlodromus pyri Scheuten is presented. The model is driven by daily maximum and minimum temperatures, and requires the per-leaf densities of both mites in spring to start each simulation. It was successful at predicting the general change in mite populations, and the peak prey density, but deviations from field results occurred at low prey density. Simulations have suggested that the present miticide spray thresholds used in New Zealand are too conservative and have also provided further insight into integrated control ofP. ulmi.     

Washing technique for monitoring mites in apple orchards

A shake-and-wash technique for monitoring the predatory phytoseiid mitesTyphlodromus pyri, Amblyseius finlandicus, and their prey,Panonychus ulmi, Tetranychus urticae andAculus schlechtendali in commercial apple orchards was developed. The removal and recovery of mites from leaves, shoots and spurs is based on agitating the plant material by hand in alcohol and subsequently removing the mites using a separating funnel. The mites are quickly killed and easily washed off the plant material, and are thus well preserved for further study. The technique is more efficient than directly counting the mites on plant material under a dissection microscope and can be easily employed both in the laboratory and in the field.     

The Transfer of Typhlodromus pyri on Grape Leaves for Biological Control of Panonychus ulmi (Acari: Phytoseiidae, Tetranychidae) in Vineyards in Ontario, Canada

The phytophagous mite Panonychus ulmi Koch has become a significant problem in Ontario vineyards. We attempted to introduce and establish populations of the predatory mite Typhlodromus pyri Scheuten for P. ulmi biological control. Grape leaves were transferred from a vineyard containing T. pyri in early summer 1998, by picking leaves from a donor vineyard and attaching them onto leaves in the release vineyard where T. pyri were extremely rare. Two release treatments were used with rates of 8.5 (1×) and 25.5 (3×) mobiles per vine. In the first season, T. pyri established in similar densities in both release treatments, which were significantly higher than controls. However, there were no differences among treatments in P. ulmi densities in 1998 as a result of predator release. During summer 1999, significantly fewer P. ulmi mite-days were observed in release plots compared to the control. Amblyseius fallacis (Garman) was common throughout the release vineyard in 1998 and in 1999, but appeared on the vines too late in the season to maintain low P. ulmi densities. T. pyri appeared to out-compete A. fallacis in 1999 because A. fallacis densities were significantly lower in plots where T. pyri had been released than in control plots. We conclude that T. pyri can be effective for P. ulmi biological control in Ontario vineyards and may be introduced by transferring leaves. In Europe, transferring prunings has been the standard method of inoculating T. pyri into new vineyards. Here we show that transferring leaves is another practical method.     

Species association among predaceous and phytophagous apple mites (Acari: Eriophyidae, Phytoseiidae, Stigmaeidae, Tetranychidae)

Predator–predator, predator–prey, and prey–prey associations among nine species of mites were studied in a plot of 100 Red Delicious apple (Malus pumila Miller) trees from 1990 to 1997. In 1990, seven-year-old trees were inoculated with Panonychus ulmi (Koch), Tetranychus urticae Koch (Acari: Tetranychidae) or both, and sprayed with azinphosmethyl (alone or plus endosulfan), or nothing. The species Zetzellia mali (Ewing) (Acari: Stigmaeidae), Amblyseius andersoni Chant (Acari: Phytoseiidae), Eotetranychus sp., Bryobia rubrioculus (Scheuten) (Acari: Tetranychidae), and Aculus schlechtendali Nalepa (Acari: Eriophyidae) were already present or immigrated into plots, and Galendromus occidentalis (Nesbitt) and Typhlodromus pyri Scheuten (Acari: Phytoseiidae) were introduced. Yule's V association index was used to measure positive, neutral, or negative interspecific associations for each species pair, because of its robustness with spatially autocorrelated data. We found that pesticide and release treatments did not greatly affect the association results, but there were strong seasonal differences. Predator–predator associations were the strongest and most consistent, showing negative associations in the early and mid seasons, and neutral ones in late season. Negative associations of T. pyri with other predators were the strongest, which is consistent with evidence that this mite can detect other predators on a leaf. Predator–prey seasonal associations were mixed, with some positive and others negative, with most significant associations occurring in the mid season. One prey–prey interaction was positive, again in mid season, most likely because of similar habitat preferences.