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.     

Pearl bodies of Cayratia japonica (Thunb.) Gagnep. (Vitaceae) as alternative food for a predatory mite Euseius sojaensis (Ehara) (Acari: Phytoseiidae)

On the young leaves, shoots, and buds of Cayratia japonica (Thunb.) Gagnep. (Vitaceae), we observed nutritious bodies called pearl bodies and hypothesized that they are utilized by generalist predators as alternative foods. Some ambulate organisms consume pearl bodies in the wild and the predatory mite Euseius sojaensis (Ehara) (Acari: Phytoseiidae) was considered as a primary candidate. Pearl bodies promoted E. sojaensis settlement on C. japonica leaves and E. sojaensis could prey on the phytophagous mite Tetranychus kanzawai Kishida (Acari: Tetranychidae) when the predators settle on a leaf before the prey. In addition, the presence of pearl bodies did not reduce predation of E. sojaensis on T. kanzawai. This was seemingly because food quality of T. kanzawai was higher than pearl bodies. These results implied that pearl bodies on C. japonica leaves are utilized by E. sojaensis as alternative foods.     

Effect of host plants on diapause induction in immature and adult <Emphasis Type="Italic">Tetranychus kanzawai</Emphasis> (Acari: Tetranychidae)

I determined the difference in sensitivity of immature and adult mites to host plants with regard to diapause induction. I used immature and adult polyphagous spider mites, Tetranychus kanzawai Kishida (Acari: Tetranychidae), and two host plants, Orixa japonica Thunb. (Rutaceae) and Phaseolus vulgaris L. (Fabaceae). The diapause incidence was investigated in two adult mite-host and two immature mite-host combinations of treatments. The incidence of diapause induction was much higher in mites developing on O. japonica than those on P. vulgaris, whichever host plants they fed on in adulthood. The host plants affected adult mites to a much lesser extent than the immature mites, though the mites feeding on O. japonica showed a consistently higher diapause incidence. These results suggest that host plants affect diapause induction to a greater extent in immature mites than in adult mites.     

Potential lethal and non-lethal effects of predators on dispersal of spider mites

Predators can affect prey dispersal lethally by direct consumption or non-lethally by making prey hesitate to disperse. These lethal and non-lethal effects are detectable only in systems where prey can disperse between multiple patches. However, most studies have drawn their conclusions concerning the ability of predatory mites to suppress spider mites based on observations of their interactions on a single patch or on heavily infested host plants where spider mites could hardly disperse toward intact patches. In these systems, specialist predatory mites that penetrate protective webs produced by spider mites quickly suppress the spider mites, whereas generalist predators that cannot penetrate the webs were ineffective. By using a connected patch system, we revealed that a generalist ant, Pristomyrmex punctatus Mayr (Hymenoptera: Formicidae), effectively prevented dispersal of spider mites, Tetranychus kanzawai Kishida (Acari: Tetranychidae), by directly consuming dispersing individuals. We also revealed that a generalist predatory mite, Euseius sojaensis Ehara (Acari: Phytoseiidae), prevented between-patch dispersal of T. kanzawai by making them hesitate to disperse. In contrast, a specialist phytoseiid predatory mite, Neoseiulus womersleyi Schicha, allowed spider mites to escape an initial patch, increasing the number of colonized patches within the system. Our results suggest that ants and generalist predatory mites can effectively suppress Tetranychus species under some conditions, and should receive more attention as agents for conservation biological control in agroecosystems.     

Arrestment response of the predatory mite Amblyseius longispinosus to Schizotetranychus nanjingensis webnests on bamboo leaves (Acari: Phytoseiidae, Tetranychidae)

The response of the predatory mite Amblyseius longispinosus (Acari: Phytoseiidae) to the webnest of the spider mite nanjingensis (Acari: Tetranychidae) was examined using two-choice tests in the laboratory. A. longispinosus females were found significantly more often on leaves with webnests than on leaves without webnests and were often observed searching under the webbing. Because spider mites and their eggs were removed from the webnests before experiments, predators responded to stimuli associated with webbing, mite feeding damage and other residues in the webnests.     

Olfactory response of the predator <Emphasis Type="Italic">Zetzellia mali</Emphasis> to a prey patch occupied by a conspecific predator

While searching for food, predators may use volatiles associated with their prey, but also with their competitors for prey. This was tested for the case of Zetzellia mali (Ewing) (Acari: Stigmaeidae), an important predator of the hawthorn spider mite, Amphitetranychus viennensis (Zacher) (Acari: Tetranychidae), in black-cherry orchards in Baraghan, Iran. Using a Y-tube olfactometer, the response of this predatory mite was tested to odour from black-cherry leaves with a conspecific female predatory mite, either with or without a female of the hawthorn spider mite when the alternative odour came from black-cherry leaves with the hawthorn spider mite only. Female predators avoided odours from leaves with both a hawthorn spider mite and a conspecific predator, as well as leaves with a conspecific predator only. We discuss whether avoidance emerges in response to cues from the competitor/predator, the herbivore/prey or the herbivore-damaged plant.     

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.     

Functionally different predators break down antipredator defenses of spider mites

Prey that lives with functionally different predators may experience enhanced mortality risk, because of conflicts between the specific defenses against their predators. Because natural communities usually contain combinations of prey and functionally different predators, examining risk enhancement with multiple predators may help to understand prey population dynamics. It is also important in an applied context: risk enhancement with multiple biological control agents could lead to successful suppression of pests. We examined whether risk enhancement occurs in the spider mite Tetranychus kanzawai Kishida (Acari: Tetranychidae) when exposed to two predator species: a generalist ant, Pristomyrmex punctatus Mayr (Hymenoptera: Formicidae), and a specialist predatory mite, Neoseiulus womersleyi Schicha (Acari: Phytoseiidae). We replicated microcosms that consisted of spider mites, ants, and predatory mites. Spider mites avoided generalist ants by staying inside their webs on leaf surfaces. In contrast, spider mites avoided specialist predatory mites that intruded into their webs by exiting the web, which obviously conflicts with the defense against ants. In the presence of both predators, enhanced mortality of spider mites was observed. A conflict occurred between the spider mites’ defenses: they seemed to move out of their webs and be preyed upon by ants. This is the first study to suggest that risk enhancement occurs in web‐spinning spider mites that are exposed to both generalist and specialist predator species, and to provide evidence that ants can have remarkable synergistic effects on the biological control of spider mites using specialist predatory mites.     

Attraction of a generalist predator towards herbivore-infested plants

The occurrence and strength of interactions among natural enemies and herbivores depend on their foraging decisions, and several of these decisions are based on odours. To investigate interactions among arthropods in a greenhouse cropping system, we studied the behavioural response of the predatory bug Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) towards cucumber plants infested either with thrips (Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)) or with spider mites (Tetranychus urticae Koch (Acari: Tetranychidae)). In greenhouse release-recapture experiments, the predatory bug showed a significant preference for both thrips-infested plants and spider mite-infested plants over clean plants. Predatory bugs preferred plants infested with spider mites to plants with thrips. Experience with spider mites on cucumber leaves prior to their release in the greenhouse had no effect on the preference of the predatory bugs. However, this experience did increase the percentage of predators recaptured. Y-tube olfactometer experiments showed that O. laevigatus was more attracted to odours from plants infested with spider mites than to odours from clean plants. Thus, O. laevigatus is able to perceive odours and may use them to find plants with prey in more natural conditions. The consequences of the searching behaviour for pest control are discussed.     

Voluntary Falling in Spider Mites in Response to Different Ecological Conditions at Landing Points

We examined voluntary-falling behaviour by adult females of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) and one of its major predators Neoseiulus californicus McGregor (Acari: Phytoseiidae). Experiments were conducted using a setup in which mites could only move onto one of two landing points by falling. Significantly more T. urticae females fell onto available food leaves compared to non-food or heavily infested leaves, whereas significantly fewer females fell onto leaves with the predatory mite N. californicus compared to leaves without the predator. This suggests that spider mites can actively choose on which patch to land on the basis of food quality and predation risk on the patch. Using the same experimental setup, starved N. californicus females never fell, suggesting that falling T. urticae females gain the potential advantage of predator avoidance.     

Intraguild predation among the predatory mites Amblyseius eharai,Amblyseius cucumeris and Amblyseius barkeri

Predator species with the same prey interact not only by competition for food and space but also by intraguild predation (IGP). The impact of IGP on introduced phytoseiid mites and native species in the context of biological control is a matter of considerable debate. Amblyseius eharai is the dominant native citrus species in central China, while Amblyseius cucumeris and Amblyseius barkeri are candidates for importation. All three species can feed on the spider mite Panonychus citri, which is the main pest in citrus. This study investigated, in the laboratory, possible IGP among these species in the absence and presence of P. citri, respectively. IGP in different densities of shared prey and intraguild (IG) prey was also studied. All three species consumed heterospecific larvae and eggs but not adults, and the IGP rate of larvae was significantly higher than that of eggs in the absence of shared prey. Additionally, the IGP rate of each group was reduced dramatically in the presence of both shared and IG prey when compared to the absence of shared prey. This occurs most likely because the three species prefer to feed on their natural prey P. citri, rather than on IG prey. Our results showed that A. eharai seems to be a more voracious IG predator than A. cucumeris. A. eharai was much more prone to IGP than A. barkeri.     

Diet‐dependent intraguild predation between the predatory mites Neoseiulus californicus and Neoseiulus cucumeris

Based on the hypothesis that matching diets of intraguild (IG) predator and prey indicate strong food competition and thus intensify intraguild predation (IGP) as compared to non‐matching diets, we scrutinized diet‐dependent mutual IGP between the predatory mites Neoseiulus cucumeris and N. californicus. Both are natural enemies of herbivorous mites and insects and used in biological control of spider mites and thrips in various agricultural crops. Both are generalist predators that may also feed on plant‐derived substances such as pollen. Irrespective of diet (pollen or spider mites), N. cucumeris females had higher predation and oviposition rates and shorter attack latencies on IG prey than N. californicus. Predation rates on larvae were unaffected by diet but larvae from pollen‐fed mothers were a more profitable prey than those from spider‐mite fed mothers resulting in higher oviposition rates of IG predator females. Pollen‐fed protonymphs were earlier attacked by IG predator females than spider‐mite fed protonymphs. Spider mite‐fed N. californicus females attacked protonymphs earlier than did pollen‐fed N. californicus females. Overall, our study suggests that predator and prey diet may exert subtle influences on mutual IGP between bio‐control agents. Matching diets did not intensify IGP between N. californicus and N. cucumeris but predator and prey diets proximately influenced IGP through changes in behaviour and/or stoichiometry.     

Non-destructive direct polymerase chain reaction (direct PCR) greatly facilitates molecular identification of spider mites (Acari: Tetranychidae)

Spider mites (Acari: Tetranychidae) include serious agricultural pests and some species have spread globally as invasive species.. For this reason, rapid and simple identification of spider mite species is necessary for agricultural field and plant quarantine inspection. DNA sequence-based molecular techniques can rapidly identify spider mites. However, extracting DNA from minute invertebrates is difficult, expensive and time consuming. Here, we describe a polymerase chain reaction (PCR) technique in which the whole body of a spider mite adult is non-destructively soaked in PCR solution. The mite is then removed intact and can be used as a voucher specimen, leaving the PCR solution as the template and avoiding the need for a DNA extraction kit. For this study, we used six common spider mite species from four genera [Tetranychus urticae Koch (red form), Tetranychus kanzawai Kishida, Tetranychus parakanzawai Ehara, Oligonychus gotohi Ehara, Eotetranychus smithi Pritchard & Baker and Panonychus citri (McGregor)]. A portion of the mitochondrial cytochrome c oxidase subunit I (COI) gene was amplified with a universal primer pair from all individuals examined and sequenced. This method shortened the time for molecular identification from 9 to 5 h and eliminated the cost of commercial kits for DNA extraction [ca. 600 yen (~5.3 USD) per sample].     

Predatory role of Neoseiulus fallacis (Acari: Phytoseiidae): spatial and temporal dynamics in Washington red raspberry fields

The seasonal abundance of spider mites and their predator Neoseiulus fallacis (Garman) (Acari: Phytoseiidae) was determined during three consecutive years in Washington State red raspberry fields. Tetranychus urticae Koch (Acari: Tetranychidae), Eotetranychus carpini borealis (Ewing) (Acari: Tetranychidae), and N. fallacis were commonly found in Skagit and Whatcom Counties. E. carpini borealis colonized the fruiting canes earlier in the season than T. urticae. The two phytophages overlapped in midseason, but T. urticae entered diapause earlier than E. carpini borealis and N. fallacis. Densities of N. fallacis increased with increase in spider mite densities. However, the numerical response of the predator was more evident for T. urticae than for E. carpini borealis. Nevertheless, the predator was spatially associated with the two prey species. The spatial and seasonal distribution of N. fallacis in relationship to host plant phenology and prey distribution may influence the effectiveness of this predator as a biological control agent against spider mites in red raspberry. Densities of the predator increased too late to prevent spider mite damage. The predatory role of N. fallacis could be enhanced by introducing or conserving predators that are more tolerant to climatic factors that prevail in and around the cane canopy in the beginning of the season.     

Overwintering survival and postdiapause fecundity in a population of the Kanzawa spider mite <Emphasis Type="Italic">Tetranychus kanzawai</Emphasis> (Acari: Tetranychidae) on <Emphasis Type="Italic">Orixa japonica</Emphasis> (Rutaceae)

In several adult-diapausing insects and mites, long duration of diapause decreases egg production after diapause termination. However, such nonlethal effects are much less studied than overwintering survival. In this study, lethal and nonlethal effects of different periods of diapause were investigated in an adult-diapausing spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae), through field experiments. Diapausing females produced in the laboratory were kept in their natural habitat from October or November to the next April, and survival rate and postdiapause fecundity were compared between the months. The survival rate was lower, but not significantly, in the October treatment. Postdiapause fecundity was also not significantly different between the months. These results suggest that the effects of diapause on survival and reproduction are quite small after October, when diapausing mites are increasing in their natural habitat.     

Kanzawa spider mites acquire enemy‐free space on a detrimental host plant,oleander

Studies have proposed that predators of herbivores suffer significant fitness losses from the defense chemicals of host plants, and that herbivores adapted to these chemicals may experience reduced predation risk when residing on such plant species. We examined the effects of oleander, Nerium indicum Mill. (Apocynaceae), a host plant of the spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae), on their prime predator, Neoseiulus womersleyi (Schicha) (Acari: Phytoseiidae), and tested the hypothesis that this host plant provides enemy‐free space. At the study sites, T. kanzawai occurred on oleander shrubs; in contrast, although N. womersleyi was present in the area, no individuals were found on oleander. Tetranychus kanzawai feeding on oleander negatively affected the settlement, development, and egg production of N. womersleyi. The lower egg production was a result of both the direct effects of oleander and the indirect effects via T. kanzawai. Previous studies showed that the fitness of T. kanzawai in the presence of N. womersleyi was lower than that in the absence of the predator, and lower on oleander than on other palatable host plant species in the absence of predators. Our findings suggest that N. womersleyi may not be able to invade T. kanzawai patches on oleander shrubs, which results in the fitness of T. kanzawai being higher on oleander than on other host plant species in the same area when N. womersleyi is present. This supports the hypothesis that T. kanzawai acquires enemy‐free space on oleander using the direct and indirect adverse effects of oleander on their predators as major defense mechanisms.     

Biological control of the citrus red mite <Emphasis Type="Italic">Panonychus</Emphasis><Emphasis Type="Italic">citri</Emphasis> by the predator mite <Emphasis Type="Italic">Typhlodromus athiasae</Emphasis> on two citrus cultivars under greenhouse conditions

This study examined the efficacy of the predatory mite Typhlodromus athiasae Porath and Swirski (Acari: Phytoseiidae) as a biological control agent of the citrus red mite Panonychus citri (McGregor) (Acari: Tetranychidae) on seedlings of Washington and Valencia citrus cultivars at 1:10, 1:20 and 1:40 predator:prey release ratios under greenhouse conditions. At predator:prey ratios of 1:10, significant reductions on P. citri populations were observed one week after release of T. athiasae, and populations remained at low levels thereafter. The highest mean numbers of P. citri were found in the third week on the Washington cultivar and in the fourth week on Valencia, in a control group with no predators. This study demonstrates the potential of T. athiasae to effectively control P. citri on Washington and Valencia cultivars under greenhouse conditions at predator:prey ratios of 1:10. However, T. athiasae was unable to control the citrus red mite populations when the predator:prey ratio was reduced to 1:40. We therefore recommend a release ratio of 1:10 for effective control of P. citri in greenhouses on seedlings of Washington and Valencia citrus.     

Spatial distribution of predators and prey affect biological control of twospotted spider mites by Phytoseiulus persimilis in greenhouses

We evaluated the effects of predator release pattern and prey distribution on rate of suppression of the twospotted spider mite, Tetranychus urticae Koch (Acari, Tetranychidae) and visual damage to the ornamental plant, Impatiens wallerana Hook.f., in a greenhouse. Sixteen impatiens plants were arranged in a square and infested with the same total number of spider mites distributed either evenly (equal numbers on all plants) or clumped (divided equally among the 4 central plants), simulating a “hot spot.” The predatory mite, Phytoseiulus persimilis Athias-Henriot, was released at a 1:4 predator:prey ratio based on total spider mites in the experimental unit, but the pattern of release was either even or clumped, which simulated broadcast or point-release strategies, respectively. Nine days after predator release, spider mite populations were reduced in all treatments, but only in the clumped pest-clumped predator treatment were spider mites undetectable. Poorest pest suppression occurred in the clumped spider mite-even predator treatment. Eighteen days after predator release, spider mites were eliminated in all treatments, but a reduction in average plant damage occurred only in treatments in which the predator release pattern matched the spider mite distribution (i.e., even-even or clumped-clumped) with the greatest reduction in the even-even treatment. Results suggest that there is an advantage to releasing predators in “hot spots” provided that the recommended predator:prey ratio is maintained within infested patches. If more uniform predator releases are planned, overall predator numbers need to be kept sufficiently high so that the predator:prey ratio of 1:4 shown to prevent damage on impatiens is achieved in higher-density spider mite patches.     

Conditioned olfactory responses of a predatory mite, Neoseiulus womersleyi, to volatiles from prey-infested plants

To clarify the prey‐finding behavior of the predatory mite Neoseiulus womersleyi (Schicha) (Acari: Phytoseiidae), we studied its olfactory responses to volatiles from the prey‐infested plant on which the mites had been collected. We used a local N. womersleyi population called Kanaya collected from tea (Camellia sinensis L.) (Theaceae) plants infested by Tetranychus kanzawai Kishida (Acari: Tetranychidae) in Kanaya City, Japan. Neoseiulus womersleyi (Kanaya population) were more attracted to volatiles from tea plants infested with five female T. kanzawai per leaf for 7 days than to intact tea leaves in a Y‐tube olfactometer. Tetranychus kanzawai‐induced tea leaf volatiles were identified as (E)‐β‐ocimene, (E)‐4,8‐dimethyl‐1,3,7‐nonatriene, and (E,E)‐α‐farnesene. As olfactory responses are known to differ among local populations of N. womersleyi, we compared the responses of the Kanaya population with those of a Kikugawa population collected from tea plants infested by T. kanzawai in Kikugawa City. To test the influence of previous predation experience, we reared the two populations on tea plants infested by T. kanzawai or on kidney bean plants (Phaseolus vulgaris) infested by Tetranychus urticae Koch. The Kanaya population was more attracted to the volatiles from infested plants on which they had been reared. Because the Kanaya population was not attracted to the plant volatiles they had not previously experienced, the positive response to previously experienced volatiles might be the result of learning. By contrast, the Kikugawa population showed no preference for previously experienced volatiles from infested plants. The implications of this flexibility in foraging behavior are discussed.     

Continental dispersal of the cassava green mite,an exotic pest in Africa,and implications for biological control

The continental dispersal of an exotic spider mite species is described for the first time. The cassava green mite,Mononychellus tanajoa (Bondar) (Acari: Tetranychidae), has been found to be dispersed across the cassava belt of Africa in less than 10 years after first being discovered in 1971. This mite disperses within plants by walking, and within and between fields by drifting aerially. Widespread transportation of mite-infested plant material, however, is proposed to explain the rapid spread ofM. tanajoa in Africa. Observations of mite-infested plant material being transported in the field, and laboratory evidence of mite populations surviving up to 60 days on cassava stems removed from the field and isolated from external contaminates, support this hypothesis. The spread ofM. tanajoa in Africa as a model for future introductions on cassava suggests a pattern of movement at species-specific rates. Exotic natural enemies ofM. tanajoa, especially phytoseiid predators, are expected to spread at a rate slower than their host; consequently, large-scale and long-range releases will be needed to accelerate their spread.