Inter‐ and intraspecific variation of spider mite susceptibility to fungal infections: Implications for the long‐term success of biological control

Spider mites are severe pests of several annual and perennial crops worldwide, often causing important economic damages. As rapid evolution of pesticide resistance in this group hampers the efficiency of chemical control, alternative control strategies, such as the use of entomopathogenic fungi, are being developed. However, while several studies have focused on the evaluation of the control potential of different fungal species and/or isolates as well as their compatibility with other control methods (e.g., predators or chemical pesticides), knowledge on the extent of inter‐ and intraspecific variation in spider mite susceptibility to fungal infection is as yet incipient. Here, we measured the mortality induced by two generalist fungi, Beauveria bassiana and Metarhizium brunneum, in 12 spider mite populations belonging to different Tetranychus species: T. evansi, T. ludeni, and T. urticae (green and red form), within a full factorial experiment. We found that spider mite species differed in their susceptibility to infection by both fungal species. Moreover, we also found important intraspecific variation for this trait. These results draw caution on the development of single strains as biocontrol agents. Indeed, the high level of intraspecific variation suggests that (a) the one‐size‐fits‐all strategy may fail to control spider mite populations and (b) hosts resistance to infection may evolve at a rapid pace. Finally, we propose future directions to better understand this system and improve the long‐term success of spider mite control strategies based on entomopathogenic fungi.     

Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae)

The commercially available strains of Phytoseiulus persimilis Athias-Henriot, the biological control agent of Tetranychus urticae Koch, perform poorly in the Western Mediterranean, probably because they are not well adapted to local climatic conditions. For that reason, efforts are being focused on the development of a biological control programme using native phytoseiid mites. Four species of red spider mites can be found in vegetable crops in eastern Spain: T. urticae, Tetranychus turkestani Ugarov and Nikolski, Tetranychus ludeni Zacher and the recently introduced Tetranychus evansi Baker and Pritchard. To evaluate their potential role as biological control agents, the present study evaluates the life-history of local populations of Neoseiulus californicus (McGregor) and P. persimilis when fed on T. urticae, T. turkestani, T. evansi, and T. ludeni in the laboratory. Results indicate that N. californicus and P. persimilis are able to feed and complete their development on the four tested red spider mite species. The predators may exhibit a particularly high capacity for population increase when fed on T. urticae, T. turkestani, and T. ludeni, thus may be able to provide effective control of these species in the field. When fed T. evansi, however, predator performance was poor; significant increase in development and preoviposition times, and a reduction in oviposition period and fecundity were recorded. The resultant low capacity for population growth suggests poor ability of the two tested predators to suppress T. evansi populations on commercial crops. It is unlikely therefore that P. persimilis and N. californicus, now being widely used to control T. urticae in greenhouse crops in Central Europe, will be able to halt any spread of T. evansi to greenhouse crops in temperate areas.     

Survey of natural enemies of spider mites (Acari: Tetranychidae) in citrus orchards in eastern Spain

Field surveys were conducted from 2004 to 2007 to determine the species composition and relative abundance of natural enemies associated with colonies of either the citrus red mite, Panonychus citri, or the two spotted spider mite, Tetranychus urticae, in Valencian citrus orchards (eastern Spain). Fourteen species were recorded, six phytoseiid mites and eight insect predators. Two of them are reported for the first time on citrus in Spain and two more are first reports as predators associated with T. urticae. The community of predators associated with T. urticae and P. citri was almost identical, and the Morisita–Horn index of similarity between both natural enemy complexes was close to one, suggesting that predators forage on both pest species. Quantifying the presence of many known spider mites predators in Valencian citrus orchards is an important first step towards spider mite control. A challenge for future studies will be to establish conservation and/or augmentation management strategies for these predators, especially to improve T. urticae biological control.     

The pest status and distribution of three cryptic blue oat mite species (Penthaleus spp.) and redlegged earth mite (Halotydeus destructor) in southeastern Australia

Earth mites are pests of crops and pastures in southeastern Australia.Recent studies show differences between earth mite species in their mode ofreproduction, preferred hosts and pesticide tolerance. This paper examines thedistribution and pest status of each species. The southeastern Australiandistribution for each species is mapped, incorporating new data from easternNewSouth Wales, South Australia and Tasmania. A new population of an undescribedspecies previously identified from northwestern Victoria was found in northernNew South Wales. CLIMEX was used to identify climatic factors limiting thedistribution of P. major and P.falcatus, the most broadly distributed species. This analysissuggests tolerance to heat and desiccation limits the inland distribution ofthese two species. A three-year survey of agricultural outbreaks indicates thatall Penthaleus species are major agricultural pestsalthough their pest status on crop types appears to differ. All speciescontributed to chemical control failures. However P.falcatus, previously identified in laboratory tests as havingincreased tolerance to pesticides, was the most common species associated withcontrol failures. A laboratory experiment indicated that mites are sometimespests on crops on which they cannot persist for a generation. Results arediscussed with respect to management of these agricultural pests.     

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.     

Resistance status of the carmine spider mite,Tetranychus cinnabarinus and the twospotted spider mite,Tetranychus urticae to selected acaricides on strawberries

The carmine spider mite, Tetranychus cinnabarinus (Boisduval) and the twospotted spider mite, Tetranychus urticae Koch, are serious pests of strawberries and many other horticultural crops. Control of these pests has been heavily dependent upon chemical acaricides. Objectives of this study were to determine the resistance status of these two pest species to commonly used acaricides on strawberries in a year‐round intensive horticultural production region. LC₉₀ of abamectin for adult carmine spider mites was 4% whereas that for adult twospotted spider mites was 24% of the top label rate. LC_90s of spiromesifen, etoxazole, hexythiazox and bifenazate were 0.5%, 0.5%, 1.4% and 83% of their respective highest label rates for carmine spider mite eggs, 0.7%, 2.7%, 12.1% and 347% of their respective highest label rates for the nymphs. LC_90s of spiromesifen, etoxazole, hexythiazox and bifenazate were 4.6%, 11.1%, 310% and 62% of their respective highest label rates for twospotted spider mite eggs, 3%, 13%, 432,214% and 15% of their respective highest label rates for the nymphs. Our results suggest that T. cinnabarinus have developed resistance to bifenazate and that the T. urticae have developed resistance to hexythiazox. These results strongly emphasize the need to develop resistance management strategies in the region.     

Influence of dispersal from almonds on the population dynamics and acaricide resistance frequencies of spider mites infesting neighboring cotton

Neighboring almond and cotton fields were sampled for spider mites in four locations in the San Joaquin Valley of California. The dominant species in the almonds wasTetranychus pacificus McGregor. In three cotton sites.T. pacificus was present in significantly higher densities near the almonds on at least one sampling date. In contrast.T. urticae Koch andT. turkestani Ugarov & Nikolski were equally abundant across the cotton fields. Almonds appeared to act as a continuous early-season source ofT. pacificus for cotton, with peaks in aerial dispersal from almonds occurring due to overcrowding, plant water stress, and applications of repellent acaricides. Cotton, which experienced little water stress, supported very high densities of spider mites and so acted primarily as a sink for spider-mite dispersal from almonds and other field crops throughout the growth-season. The frequencies of resistance expressed byT. pacificus andT. urticae were similar between neighboring crops, even if the acaricide had been registered for use only in almonds (cyhexatin) or cotton (dicofol). Thus, longterm acaricide selection and movement of spider mites between the two crops resulted in similar proportions of resistant individuals. In these study sites, large-scale dispersal ofT. pacificus from almonds rarely directly affected acaricide efficacy in cotton, because resistance frequencies were similar for spider mites from the two crops and because acaricide applications were usually made in cotton after dispersal from almonds was completed. In two cotton sites, field selection with dicofol was reversed by subsequent immigration of spider mites from neighboring field crops.     

Species composition of thrips (Thysanoptera: Thripidae) and spider mites (Acari: Tetranychidae) on cultivated chrysanthemum (Asteraceae) in Okinawa,southwestern Japan

We investigated the species composition of phytophagous thrips and spider mites on cultivated chrysanthemum in Okinawa, southwestern Japan. Eight thrips species belonging to the genera Frankliniella, Microcephalothrips, Scirtothrips and Thrips were found on chrysanthemum leaves. Among them, Thrips nigropilosus was the predominant species irrespective of season, island or cultivation environment (meshed greenhouse or open field), with its infestation frequency being 89% of the fields in which thrips occurred. This high frequency of occurrence suggests that T. nigropilosus is a major pest of chrysanthemum in Okinawa, even though this species has rarely been regarded as an important pest of chrysanthemum or other crops in any other areas. Thrips palmi was the second most dominant (infestation frequency 36%) and other species were scarce (<14%). Tetranychus urticae (green form) was the only tetranychid species on chrysanthemum in our survey. This lack of diversity among spider mites on chrysanthemum is peculiar considering that eight Tetranychus species have been found on vegetables in the same area. Since T. urticae (green form) has been shown to be resistant to a number of pesticides, severe pesticide applications might have simplified the spider mite fauna on chrysanthemum in Okinawa.     

Die Feinde der Raubmilben als Reduzierender Faktor der Spinnmilben

Summary The relations betweenMetatetranychus ulmi living on apple trees and its different predators are complex. The most important natural enemy of this spider mite is the predacious miteTyphlodromus pyri (= T. tiliae). It destroys more spider mites than the beneficial insects do. In the district of Stuttgart-Hohenheim about 38 species of insects and spiders feed onTyphlodromus mites. For instanceT. pyri is reduced considerably byOrius minutus. This bug is a natural enemy of aphids and spider mites, however it prefers the predatory mites. It attacks the spider mites and aphids only ifTyphlodromus mites are not available.Chrysopa vulgaris andAnthocoris nemorum are similar in their feeding habits. These two destroyTyphlodromus pyri also but they are less important thanO. minutus. The other beneficial insects in our orchards have little effect on spider mites or predacious mites. If we have enough pests on our apple trees to make spraying necessary, we should look forTyphlodromus mites and be careful no to destroy them. We should always examine the composition of the biocoenosis applying chemical agents because the populations of insects and predacious mites may vary from one area to the other.      

Diseases of Mites

An overview is given of studies on diseases of mites. Knowledge of diseases of mites is still fragmentary but in recent years more attention has been paid to acaropathogens, often because of the economic importance of many mite species. Most research on mite pathogens concerns studies on fungal pathogens of eriophyoids and spider mites especially. These fungi often play an important role in the regulation of natural mite populations and are sometimes able to decimate populations of phytophagous mites. Studies are being conducted to develop some of these fungi as commercial acaricides.Virus diseases are known in only a few mites, namely, the citrus red mite and the European red mite. In both cases, non-occluded viruses play an important role in the regulation of mite populations in citrus and peach orchards, respectively, but application of these viruses as biological control agents does not seem feasible. A putative iridovirus has been observed in association with Varroa mites in moribund honeybee colonies. The virus is probably also pathogenic for honeybees and may be transmitted to them through this parasitic mite.Few bacteria have been reported as pathogens of the Acari but in recent years research has been concentrated on intracellular organisms such as Wolbachia that may cause distorted sex ratios in offspring and incompatibility between populations. The role of these organisms in natural populations of spider mites is in particular discussed. The effect of Bacillus thuringiensis on mites is also treated in this review, although its mode of action in arthropods is mainly due to the presence of toxins and it is, therefore, not considered to be a pathogen in the true sense of the word.Microsporidia have been observed in several mite species especially in oribatid mites, although other groups of mites may also be affected. In recent years, Microsporidia infections in Phytoseiidae have received considerable attention, as they are often found in mass rearings of beneficial arthropods. They affect the efficacy of these predators as biological control agent of insect and mite pests. Microsporidia do not seem to have potential for biological control of mites.     

Which predatory mite can control both a dominant mite pest,Tetranychus urticae,and a latent mite pest,Eotetranychus asiaticus,on strawberry?

After biological control of Tetranychus urticae using Phytoseiulus persimilis, a latent mite pest, Eotetranychus asiaticus, was found on strawberries growing in a plastic greenhouse in western Japan. To determine whether the release ofP. persimilis, an exotic natural enemy of T.urticae, enhanced the occurrence of the latent pest, the efficiency of P. persimilis in controlling E.asiaticus was compared with the efficiency of two indigenous phytoseiid mites, Amblyseius californicus and A. womersleyi, under laboratory conditions. Phytoseiuluspersimilis and A. californicus attacked not onlyT. urticae but also E. asiaticus. However, the predators produced very few eggs and their offspring rarely reached adulthood when fed on E. asiaticus, so their potential as control agents for the latent mite appears to be low. In contrast, A.womersleyi feeding on E. asiaticus reproduced as well as when fed on T. urticae, and exterminated both species of spider mite. This suggests that A. womersleyihas greater potential as a biological control agent in crops where both species may occur. This revised version was published online in August 2006 with corrections to the Cover Date.     

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.     

Amensalism via webs causes unidirectional shifts of dominance in spider mite communities

Competitive displacement is considered the most severe consequence of interspecific competition; if a superior competitor invades the habitat of an inferior species, the inferior species will be displaced. Most displacements previously reported among arthropods were caused by exotic species. The lack of investigation of displacement among native species may be due to their apparently harmonious coexistence, even if it is equivalent to an outcome of interspecific association. A seasonal change in the species composition of spider mites, from Panonychus ulmi to Tetranychus urticae, is observed in apple trees worldwide. Previous laboratory experiments have revealed amensal effects of T. urticae on P. ulmi via their webs. Using manipulation experiments in an orchard, we tested whether this seasonal change in species composition occurred as the result of interspecific competition between these spider mites. Invasion by T. urticae prevented an increase in P. ulmi densities throughout the experimental periods. Degree of overlap relative to the independent distribution on a leaf-surface basis (ω _S) changed from positive to negative with increasing density of T. urticae. T. urticae invasion drove P. ulmi toward upper leaf surfaces (competitor-free space). The niche adjustment by P. ulmi occurred between leaf surfaces but not among leaves. Our findings show that asymmetrical competition between T. urticae and P. ulmi plays an important role in this unidirectional displacement and that the existence of refuges within a leaf produces the apparently harmonious coexistence of the mites and obscures their negative association.     

Geographic distribution of phytoseiid mite species (Acari: Phytoseiidae) on crops in Okinawa,a subtropical area of Japan

We extensively identified phytoseiid mites co‐occurring with spider mites on crops throughout the islands of Okinawa, southwestern Japan to obtain fundamental information for controlling spider mites in the area using natural enemies. Of the 19 species found, three were new to Japan and eight were new to Okinawa. Neoseiulus womersleyi was the most common species with respect to the distribution range. Following N. womersleyi, six species including Amblyseius eharai were common, whereas N. californicus was not, suggesting that the recent change in dominant species from N. womersleyi to N. californicus observed on the main islands of Japan had not happened in Okinawa. On one small island (Tarama Island) located in the southwestern part of Okinawa, N. womersleyi was not found, and instead N. longispinosus, which is morphologically similar to N. womersleyi and has not been found in Japan, occurred. This suggests interisland differences in the relative frequencies of N. womersleyi and N. longispinosus in Okinawa.     

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.     

Biology, ecology and control of the Penthaleus species complex (Acari: Penthaleidae)

Blue oat mites, Penthaleus spp. (Acari: Penthaleidae), are major agricultural pests in southern Australia and other parts of the world, attacking various pasture, vegetable and crop plants. Management of these mites has been complicated by the recent discovery of three cryptic pest species of Penthaleus, whereas prior research had assumed a single species. The taxonomy, population genetics, ecology, biology and control of the Penthaleus spp. complex are reviewed. Adult Penthaleus have a dark blue-black body approximately 1 mm in length, and eight red-orange legs. Within Australia, they are winter pests completing two or three generations a season, depending on conditions. The summer is passed as diapausing eggs, when long-distance dispersal is thought to occur. The Penthaleus spp. reproduce by thelytokous parthenogenesis, with populations comprising clones that differ ecologically. The three pest Penthaleus spp. differ markedly in their distributions, plant hosts, timing of diapause egg production and response to pesticides, highlighting the need to develop control strategies that consider each species separately. Chemicals are the main weapons used in current control programs, however research continues into alternative more sustainable management options. Host plant resistance, crop rotations, conservation of natural enemies, and improved timing of pesticide application would improve the management of these pests. The most cost-effective and environmentally acceptable means of control will result from the integration of these practices combined with the development of a simple field-based kit to distinguish the different mite species.     

Biological control of thrips and whiteflies by a shared predator: Two pests are better than one

We studied the capacity of one species of predator to control two major pests of greenhouse crops, Western flower thrips (Frankliniella occidentalis (Pergande)) and the greenhouse whitefly (Trialeurodes vaporariorum (Westwood)). In such a one-predator–two-prey system, indirect interactions can occur between the two pest species, such as apparent competition and apparent mutualism. Whereas apparent competition is desired because it brings pest levels down, apparent mutualism is not, because it does the opposite. Because apparent competition and apparent mutualism occurs at different time scales, it is important to investigate the effects of a shared natural enemy on biological control on a time scale relevant for crop growth. We evaluated the control efficacy of the predatory mites Amblyseius swirskii (Athias-Henriot) and Euseius ovalis (Evans) in cucumber crops in greenhouse compartments with only thrips, only whiteflies or both herbivorous insects together. Each of the two predators controlled thrips, but A. swirskii reduced thrips densities the most. There was no effect of the presence of whiteflies on thrips densities. Whitefly control by each of the two predators in absence of thrips was not sufficient, yet better with E. ovalis. However, whitefly densities in presence of thrips were reduced dramatically, especially by A. swirskii. The densities of predators were up to 15 times higher in presence of both pests than in the single-pest treatments. Laboratory experiments with A. swirskii suggest that this is due to a higher juvenile survival and developmental rate on a mixed diet. Hence, better control may be achieved not only because of apparent competition, but also through a positive effect of mixed diets on predator population growth. This latter phenomenon deserves more attention in experimental and theoretical work on biological control and apparent competition.     

Provision of astigmatid mites as supplementary food increases the density of the predatory mite Amblyseius swirskii in greenhouse crops,but does not support the omnivorous pest,western flower thrips

Astigmatid mites can be used as prey for mass rearing of phytoseiid predators, but also as a supplemental food source to support predator populations in crops. Here we evaluated the potential of six species of astigmatid mites (living or frozen) as alternative food for the predatory mite Amblyseius swirskii Athias-Henriot in greenhouse crops. All prey mites tested were suitable for predator oviposition. In general, oviposition was greater when prey mites were reared on dog food with yeast than when they were reared on wheat bran with yeast. Amongst prey items provided as frozen diet, larvae of Thyreophagus entomophagus (Laboulbene), Acarus siro L. and Lepidoglyphus destructor (Schrank) that had been reared on dog food with yeast, resulted in the highest oviposition rates of A. swirskii. T. entomophagus larvae as frozen diet resulted in the shortest preimaginal developmental time of A. swirskii. On chrysanthemum plants, we found that the greatest increase in predator density occurred when living mites of T. entomophagous were used as a food source. This increase was greater than when predators were fed cattail pollen, a commonly used supplemental food. Effects on predators of providing living A. siro and L. destructor, or frozen larvae of T. entomophagous as food, were comparable with provision of pollen. Use of supplemental food in crops can be a risk if it is also consumed by omnivorous pests such as western flower thrips, Frankliniella occidentalis Pergande. However, we showed that both frozen and living mites of T. entomophagous were unsuitable for thrips oviposition. Hence, we believe that provision of prey mite species increases A. swirskii density, supporting biological control of thrips and other pests in greenhouse crops.

     

Population‐specific effect of Wolbachia on the cost of fungal infection in spider mites

Many studies have revealed the ability of the endosymbiotic bacterium Wolbachia to protect its arthropod hosts against diverse pathogens. However, as Wolbachia may also increase the susceptibility of its host to infection, predicting the outcome of a particular Wolbachia‐host–pathogen interaction remains elusive. Yet, understanding such interactions and their eco‐evolutionary consequences is crucial for disease and pest control strategies. Moreover, how natural Wolbachia infections affect artificially introduced pathogens for biocontrol has never been studied. Tetranychus urticae spider mites are herbivorous crop pests, causing severe damage on numerous economically important crops. Due to the rapid evolution of pesticide resistance, biological control strategies using entomopathogenic fungi are being developed. However, although spider mites are infected with various Wolbachia strains worldwide, whether this endosymbiont protects them from fungi is as yet unknown. Here, we compared the survival of two populations, treated with antibiotics or naturally harboring different Wolbachia strains, after exposure to the fungal biocontrol agents Metarhizium brunneum and Beauveria bassiana. To control for potential effects of the bacterial community of spider mites, we also compared the susceptibility of two populations naturally uninfected by Wolbachia, treated with antibiotics or not. In one population, Wolbachia‐infected mites had a better survival than uninfected ones in absence of fungi but not in their presence, whereas in the other population Wolbachia increased the mortality induced by B. bassiana. In one naturally Wolbachia‐uninfected population, the antibiotic treatment increased the susceptibility of spider mites to M. brunneum, but it had no effect in the other treatments. These results suggest that natural Wolbachia infections may not hamper and may even improve the success of biological control using entomopathogenic fungi. However, they also draw caution on the generalization of such effects, given the complexity of within‐host–pathogens interaction and the potential eco‐evolutionary consequences of the use of biocontrol agents for Wolbachia‐host associations.     

Interactions in a tritrophic acarine predator-prey metapopulation system III: effects of Tetranychus urticae (Acari: Tetranychidae) on host plant condition

Spider mites are serious pests on many economically important plant species, because they may reduce plant productivity and, at high mite densities, overexploit and even kill the host plants. We have conducted a series of greenhouse experiments to quantify the effects of two-spotted spider mites (Tetranychus urticae) on host plants (Phaseolusvulgaris). The average amount of chlorophyll per cm² leaf area was used as a measure of plant condition. It was shown that chlorophyll concentration decreases with plant age and intensity of spider mite feeding. Damage caused by spider mites was assessed visually, using the Leaf Damage Index (LDI) defined by, and a mathematical relationship between the visual measurements and the amount of chlorophyll/cm² was fitted to data. The relationship may serve as a short-cut to estimate overall plant injury, expressed as the relative loss of chlorophyll/cm² leaf area caused by spider mites (D). D takes values between 0 (no injury) and 1 (all leaves dead). A highly significant positive relationship between the instantaneous spider mite density and D was found, even though D is expected to reflect the cumulated density of mites (mite-days). A model of plant growth incorporating information about plant age and D predicts that plant area has a maximum when plant age is about 60 days, and that plant area decreases exponentially with an increase in D. This revised version was published online in July 2006 with corrections to the Cover Date.