Resurgences of spider mites (Acari: Tetranychidae) induced by synthetic pyrethroids

Causes of spider mite (Acari: Tetranychidae) population resurgences consequent upon exposure to synthetic pyrethroid (SP) treatments are reviewed. Resurgences may be seen as soon as 1 week, or even as late as a whole season, post-treatment. Synthetic pyrethroids vary in their adverse effects on spider mites, and also differ in their ability to invoke resurgences of different spidermite species on diverse plants. These pesticides are lethal as well as repellent to phytoseiids and other predators that prey on spider mites, may inhibit fungi which attack the latter, and affect phytophagous competitors. Spider mites are likewise repelled by SPs, thus becoming more evenlydistributed and less web-restricted, with a resultant increase in fecundity. Spider-mite development is shortened due to SPs and the sex ratio becomes more female-biased; onset of winter diapause also seems to be delayed. Synthetic pyrethroids appear to sensitize to spider-mite infestation plants which have not hitherto been attacked. Some SP effects (whether on spider mites, natural enemies or competitors) appear to be direct, whereas others may be mediated through the host plants. The effect of SPs on the other Acari is variable within the Prostigmata and Astigmata. Most Mesostigmata and Metastigmata (ticks) are very sensitive, whilst the Cryptostigmata (Oribatei) appear to be insensitive. Synthetic pyrethroids-induced resurgences of Homoptera are comparatively reviewed, with the conclusion that some of the phenomena may be similar to those observed in spider mites. Various resurgence models are discussed, as well as the three main causes of variation (SPs, spider-mite species, host plants) in the observed phenomena. The need for more rigorous and carefully controlled experimentation is emphasized.     

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.     

Volatile spider-mite pheromone and host-plant kairomone, involved in spaced-out gregariousness in the spider mite Tetranychus urticae

ABSTRACT. From the host plant-spider mite complex Phaseolus lunatus—Tetranychus urticae Koch a volatile chemical is emitted that acts as a kairomone for the predatory mite Phytoseiulus persimilis Athias-Henriot (Sabelis et al. , 1984a). This kairomone is apparently a byproduct of a vital physiological process and/or it has a function in the biology of the spider mite as well.
The spider mite—host plant complex also emits a volatile spider-mite dispersing pheromone. This is shown in the present study where spider mites were introduced into an odour patch on a horizontal screen in a vertical airflow olfactometer. When spider-mite infested leaves of Lima bean are offered, the spider mites walk mainly straight and soon reach the edge of the screen. On the other hand, when clean Lima bean leaves are offered, the mites walk tortuously most of the time and reach the edge of the screen much later. Artificially damaged plants elicit the same response as undamaged plants. Differences in spider-mite behaviour are observed in the vertical airflow olfactometer when odour of either clean or spider-mite infested leaves is offered. A comparison of the behaviour in these two situations with that when no odour was offered suggests that Lima bean leaves emit a volatile kairomone that activates T. urticae and makes them return after losing the stimulus. A Y-tube olfactometer experiment confirms the existence of this kairomone.
At a low ratio of dispersing pheromone to plant kairomone, the spider mites behave as if only kairomone is present, walking mainly tortuously. At a high ratio they disperse. No aggregation-pheromonal effect is observed.
The possibility that the spider-mite dispersing pheromone acts as a kairomone for P. persimilis is discussed.     

Spider-Mite Problems and Control in Taiwan

Problems with spider mites first appeared in Taiwan in 1958, eight years after the importation of synthetic pesticides, and the mites evolved into major pests on many crops during the 1980s. Of the 74 spider mite species recorded from Taiwan 10 are major pests, with Tetranychus kanzawai most important, followed by T. urticae, Panonychus citri, T. cinnabarinus, T. truncatus and Oligonychus litchii. Most crops suffer from more than one species. Spider mites reproduce year-round in Taiwan. Diapause occurs only in high-elevation areas. Precipitation is the most important abiotic factor restricting spider-mite populations. Control is usually accomplished by applying chemicals. Fifty acaricides are currently registered for the control of spider mites. Acaricide resistance is a serious problem, with regional variation in resistance levels. Several phytoseiid mites and a chrysopid predator have been studied for control of spider mites with good effect. Efforts to market these predators should be intensified so that biological control can be a real choice for farmers.     

Direct and indirect effects of imidacloprid on fecundity and abundance of Eurytetranychus buxi (Acari: Tetranychidae) on boxwoods

Populations of spider mites often reach high levels on urban plants. In many cases, insecticide applications targeting other herbivores trigger outbreaks of spider mites. Recently, elevated populations of spider mites on a diversity of plants in urban landscapes have been associated with applications of imidacloprid, a neonicotinoid insecticide. Imidacloprid has also been linked to increased fecundity in two species of spider mites. In this study, we evaluated the indirect (plant-mediated) and direct impact of imidacloprid on fecundity and longevity of Eurytetranychus buxi Garman (Acari: Tetranychidae), feeding on boxwoods, Buxus sempervirens L. Moreover, we compared the abundance of E. buxi on imidacloprid-treated and untreated boxwoods in the landscape and a greenhouse to determine if changes in the fecundity of mites exposed to imidacloprid were linked to outbreaks of E. buxi. We found that females consuming imidacloprid-treated plants laid more eggs than females feeding on untreated boxwoods, while their longevity remained unchanged. Fecundity was not affected, however, when spider mites were directly sprayed with imidacloprid and consumed foliage of untreated boxwoods. Furthermore, populations of E. buxi were greater on boxwoods treated with imidacloprid in the landscape and greenhouse. On landscape boxwoods, elevated populations of E. buxi persisted into a second year. We also observed general lack of predators of spider mites on treated and untreated boxwoods in the field suggesting that imidacloprid’s eruptive effect on E. buxi stems more from indirect changes in plant quality than from a loss of top-down regulation from E. buxi’s natural enemies.     

Effects of microenvironment on the dynamics of spider-mite populations

The relationship between environmental variables (chiefly temperature and humidity) and the population dynamics of spider mites is reviewed. Both direct effects on the spider mites and indirect effects operating through effects on spider mite natural enemies (mainly phytoseiid mites) are discussed. Factors determining the environmental conditions actually experienced by spider mites (microenvironment) are presented.Microenvironmental information versus environmental information from nearby weather stations is evaluated for utility in predicting spider mite population dynamics. A comprehensive plant canopy/spider mite/phytoseiid model is used to simulate an irrigated maize/spider-mite/phytoseiid system in a semi-arid climate. Under nearly all tested combinations of weather and irrigation, substantial differences were seen between simulations that considered microenvironment and those that considered only environmental conditions above the plant canopy. Future research needs are discussed.     

Coincidental intraguild predation by caterpillars on spider mites

Intraguild predation (IGP) is defined as the killing and eating of prey species by a predator that also can utilize the resources of the prey. It is mainly reported among carnivores that share common herbivorous prey. However, a large chewing herbivore could prey upon sedentary and/or micro herbivores in addition to utilizing a host plant. To investigate such coincidental IGP, we observed the behavioral responses of the polyphagous mite Tetranychus kanzawai Kishida (Acari: Tetranychidae) when its host plant Cayratia japonica (Thunb.) Gagnep. (Vitaceae) was attacked by hornworms, Theretra japonica Boisduval (Sphingidae) and T. oldenlandiae Fabricius (Sphingidae). We also examined an interaction between the oligophagous mite Panonychus citri McGregor (Acari: Tetranychidae) and caterpillars of the swallowtail Papilio xuthus L. (Papilionidae) that share citrus plants as their main food source. Although all T. kanzawai and some active stage P. citri tried to escape from the coincidental IGP, some were consumed together with eggs, quiescent mites, and host plant leaves, suggesting that coincidental IGP occurs on spider mites in the wild. Moreover, neither hornworms nor swallowtail caterpillars distinguished between spider mite-infested and uninfested leaves, suggesting that the mite-infested leaves do not discourage caterpillar feeding. The reasons that the mites have no effective defense against coincidental IGP other than escaping are discussed.     

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.     

Bionomics ofEotetranychus tiliarium and its phytoseiid predators

Under urban conditions,Eotetranychus tiliarium (Hermann) frequently develops into high population densities onTilia lining streets, in contrast to its development in natural habitats and on park trees. In mixed forest and on park trees, a regulating system precludes these outbreaks. In an earlier study it was shown that a change in the predacious mite species composition, leading to displacement of the most effective predator species by less effective ones, is the main reason for this phenomenon.The bionomics ofE. tiliarium on its host plantTilia spp. in various habitats were studied as well as the characteristics of the predacious mites which determine their potential for preventing spider-mite outbreaks.Predacious mites from the family Phytoseiidae were able to preventE. tiliarium outbreaks.Paraseiulus soleiger was the most effective predacious mite species, because it has a short development period, a long period of longevity, a long oviposition period, and has a clear preference forE. tiliarium and a high prey-consumption capacity. Eotetranychus tiliarium onTilia lining streets has a greater potential for increase than the spider mites from park trees and from forest trees. The nutritive value of leaves on trees in street habitats is increased by the increased salt content in the soil from snow control in winter. Also, the higher temperatures in urban conditions may stimulate population development.     

Host-plant-mediated interaction between populations of a true omnivore and its herbivorous prey

Western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), are competitors with twospotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), for plant resources and potential predators on spider mites when the opportunity arises. Which interaction predominates may depend on relative population densities and individual species’ responses to the plants on which they co‐occur. We examined interactions between populations of thrips and spider mites on several cultivars of two bedding plants: impatiens (Impatiens wallerana Hook.f) cultivars ‘Impulse Orange’ and ‘Cajun Carmine’, and ivy geranium [Pelargonium peltatum (L.) L’Her ex Aiton] cultivars ‘Sybil Holmes’ and ‘Amethyst 96’. Four combinations of thrips and mite numbers were studied: thrips alone, mites alone, and two densities of thrips and mites together. We compared population numbers after 4 weeks. Overall, mite numbers increased more rapidly than thrips did, but both species increased more rapidly on impatiens than on ivy geraniums. Between impatiens cultivars, thrips and mites increased more slowly on ‘Cajun Carmine’ (i.e., it was more resistant) than on ‘Impulse Orange’. On ivy geraniums, spider mites increased more slowly on ‘Sybil Holmes’ than on ‘Amethyst 96’ but the reverse was the case for thrips. Regardless of plant species or cultivar, thrips had a strong negative effect on spider mites whenever they co‐occurred, suppressing mite population growth by around 50% compared to when mites were alone. However, the effect of spider mites on western flower thrips depended on the quality of the plant species. On impatiens, thrips co‐occurring with spider mites increased slightly more than thrips alone did, while on ivy geranium mites had a small negative effect on thrips. Contrary to expectations, thrips had a larger negative impact on spider mites on plants that were more susceptible to thrips than they did on plants more resistant to thrips. We suggest that host plants mediate the interaction between an omnivore and its herbivorous prey not only by altering individual diet choice but by changing the relative population dynamics of each species.     

Host-plant species modifies the diet of an omnivore feeding on three trophic levels

The diet choice of omnivores feeding on two adjacent trophic levels (either plants and herbivores or herbivores and predators) has been studied extensively. However, omnivores usually feed on more than two trophic levels, and this diet choice and its consequences for population dynamics have hardly been studied. We report how host-plant quality affects the diet choice of western flower thrips feeding on three trophic levels: plants (cucumber or sweet pepper), eggs of spider mites and eggs of a predatory mite that attacks spider mites. Spider mites feed on the same host plants as thrips and produce a web that hampers predator mobility. To assess the indirect effects of spider mites on predation by thrips, the thrips were offered spider-mite eggs and predatory-mite eggs on cucumber or sweet pepper leaf discs that were either clean, damaged by spider mites but without spider-mite web, or damaged and webbed. We show that, overall, thrips consumed more eggs on sweet pepper, a plant of low quality, than on cucumber, a high quality host plant. On damaged and webbed leaf discs (mimicking the natural situation), thrips killed more predator eggs than spider-mite eggs on sweet pepper, but they killed equal numbers of eggs of each species on cucumber. This is because web hampered predation on spider-mite eggs by thrips on sweet pepper, but not on cucumber, whereas it did not affect predation on predatory-mite eggs. We used the data obtained to parameterize a model of the local dynamics of this system. The model predicts that total predation by the omnivore has little effects on population dynamics, whereas differential attack of predator eggs and spider-mite eggs by the omnivore has large effects on the dynamics of both mite species on the two host plants.     

Effects of herbivory and plant conditioning on the population dynamics of spider mites

Plants vary in their resistance to tetranychid spider mites, and this can have profound effects on spider-mite population dynamics. Such variation can be attributable to many factors. In this review, however, we focus on how previous or concurrent feeding by phytophagous hervivores influences expression of plant resistance to spider mites.Induced resistance is a change in the host plant in response to extrinsic stimuli, resulting in reduced host suitability for the population growth of spider mites. We begin our review by summarizing the different ways in which spider mites and plants interact to produce induced resistance-like phenomena. We then discuss a number of hypotheses which address the mechanisms underlying induced resistance and end by suggesting agricultural applications. Although the potential use of induced resistance to manage spider mites is apparent, progress in this area will depend on a better understanding of the mechanisms involved and their associated costs and benefits to the plant.     

Diapause incidence in the two-spotted spider mite increases due to predator presence, not due to selective predation

We recently reported evidence for increased diapause incidence in the spider mite Tetranychus urticae in presence of the predatory mite Typhlodromus pyri. This effect may arise from (1) selective predation on non-diapause spider mites, (2) predator-induced diapause in spider mites, or (3) both. Using a different strain of T. urticae, we first recovered increased diapause incidence in association with predators. Then, we tested for selective feeding in two-choice experiments with equal numbers of non-diapause and diapause spider mites. We found that the predatory mite had a significant preference for the latter. This indicates that increased diapause incidence in association with predatory mites is not due to selective predation. Therefore, predator-mediated physiological induction of diapause seems a more likely explanation. The cues leading to induction appear to relate to the predators, not their effects, since predation simulated by spider-mite removal or puncturing did not significantly affect diapause incidence. Why spider mites benefit from this response, remains an open question.This revised version was published online in May 2005 with a corrected cover date.     

Does use of pesticides known to harm natural enemies of spider mites (Acari: Tetranychidae) result in increased number of miticide applications? An examination of California walnut orchards

Integrated pest management (IPM) offers guidelines to reduce spider mite (Acari: Tetranychidae) outbreaks by avoiding pesticides known to be harmful to the natural enemies of spider mites. However, in practice, these guidelines can be inconsistent in their effectiveness. The project examined whether California walnut (Juglans L.) growers, following IPM guidelines to avoid pesticides harmful to the natural enemies of spider mites, achieved lower miticide use. Significant statistical tests suggested that fields with harmful applications were 40% more likely to have a miticide application than fields without. Although the IPM guidelines achieved the goal of reducing miticide use, further analysis of other potential causal mechanisms behind outbreaks could strengthen the effectiveness of the guidelines, potentially increasing IPM adoption.     

Vector and virus induce plant responses that benefit a non-vector herbivore

The negative cross-talk between induced plant defences against pathogens and arthropod herbivores is exploited by vectors of plant pathogens: a plant challenged by pathogens reduces investment in defences that would otherwise be elicited by herbivores. This negative cross-talk may also be exploited by non-vector herbivores which elicit similar anti-herbivore defences in the plant. We studied how damage by the thrips Frankliniella occidentalis and/or infection with Tomato spotted wilt virus (TSWV) affect the performance of a non-vector arthropod: the two-spotted spider mite Tetranychus urticae, a parenchym feeder just like F. occidentalis. Juvenile survival of spider mites on plants inoculated with TSWV by thrips was higher than on control and on thrips-damaged plants. However, thrips damage did not reduce spider-mite survival as compared to the control, suggesting that the positive effect of TSWV on spider-mite survival is independent of anti-thrips defence. Developmental and oviposition rates were enhanced on plants inoculated with TSWV by thrips and on plants with thrips damage. Therefore, spider mites benefit from TSWV-infection of pepper plants, but also from the response of plants to thrips damage. We suggest that the positive effects of TSWV on this non-vector species cannot be explained exclusively by cross-talk between anti-herbivore and anti-pathogen plant defences.     

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.     

Consequences of mite feeding injury to beans on the fecundity and survivorship of the two-spotted spider mite (Acari: Tetranychidae)

Fecundity and survival of the two-spotted spider mite,Tetranychus urticae Koch, were examined on bean (Phaseolus vulgaris L.) plants that had been subjected to mite feeding injury in the laboratory. Different numbers ofT. urticae were restricted on the first two leaves of young bean plants, and spider-mite fecundity and survivorship was assayed on the third leaf. Each plant received four recently enclosed females, one female from each of four mite lineages. Using changes in the ratio of root mass to shoot mass of bean plants as a continuous measure of plant stress from spider-mite feeding, fecundity was positively related to stress for three out of four experiments. In two out of four experiments, survival of females was also positively related to stress, but reached an asymptote at slight or moderate stress levels. No evidence for induced resistance in beans was found. Mite lineage and the interaction between lineage and stress affected female survival but not fecundity. The implications of these results for understanding spider-mite outbreaks are discussed.     

The embryogenesis of the Tick Rhipicephalus (Boophilus) microplus: The establishment of a new chelicerate model system

Summary: Chelicerates, which include spiders, ticks, mites, scorpions, and horseshoe crabs, are members of the phylum Arthropoda. In recent years, several molecular experimental studies of chelicerates have examined the embryology of spiders; however, the embryology of other groups, such as ticks (Acari: Parasitiformes), has been largely neglected. Ticks and mites are believed to constitute a monophyletic group, the Acari. Due to their blood‐sucking activities, ticks are also known to be vectors of several diseases. In this study, we analyzed the embryonic development of the cattle tick, Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). First, we developed an embryonic staging system consisting of 14 embryonic stages. Second, histological analysis and antibody staining unexpectedly revealed the presence of a population of tick cells with similar characteristics to the spider cumulus. Cumulus cell populations also exist in other chelicerates; these cells are responsible for the breaking of radial symmetry through bone morphogenetic protein signaling. Third, it was determined that the posterior (opisthosomal) embryonic region of R. microplus is segmented. Finally, we identified the presence of a transient ventral midline furrow and the formation and regression of a fourth leg pair; these features may be regarded as hallmarks of late tick embryogenesis. Importantly, most of the aforementioned features are absent from mite embryos, suggesting that mites and ticks do not constitute a monophyletic group or that mites have lost these features. Taken together, our findings provide fundamental common ground for improving knowledge regarding tick embryonic development, thereby facilitating the establishment of a new chelicerate model system. genesis 51:803–818. © 2013 Wiley Periodicals, Inc.     

A comparison of the toxic and sub-lethal effects of fluvalinate and esfenvalerate on the twospotted spider mite (Acari: Tetranychidae)

There was no difference in the direct toxicity of fluvalinate and esfenvalerate to twospotted spider mite (TSSM), Tetranychus urticae Koch. adults. The residual toxicity LC₅₀ of esfenvalerate was lower. Neither pyrethroid was toxic (<10% mortality) to TSSM eggs or adults at their recommended field concentrations. Fluvalinate was twice as toxic (45% mortality) than esfenvalerate to TSSM larvae at 0.01 g.a.i L^-1. The toxicity of the pyrethroids to TSSM protonymphs and deutonymphs was similar (16–28% mortality at 0.1 g a.i. L^-1). Dispersal from the treated surface was the main response to both pyrethroids by TSSM protonymphs, deutonymphs and adults. Maximum run-off by TSSM adults from fluvalinate and esfenvalerate treated surfaces was found with 0.01 and 0.005 g a.i. L^-1 respectively. Spin-down from pyrethroid treated surfaces was positively correlated with concentration. Oviposition was negatively correlated with concentration. Fluvalinate caused greater reductions in oviposition than esfenvalerate. Both pyrethroids reduced TSSM development rate from larval, protonymph and deutonymph stages, but fluvalinate caused larger reductions. Both pyrethroids prevented mating: for ten days oviposition 93% and 98% of offspring were male for esfenvalerate and fluvalinate respectively at 0.1 g a.i. L^-1. These findings are discussed with respect to the incidence of pyrethroid induced mite outbreaks.