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

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

Comparative life-history traits of three phytoseiid mites associated with Tetranychus urticae (Acari: Tetranychidae) colonies in clementine orchards in eastern Spain: implications for biological control

The management of Tetranychus urticae, a key pest of clementine trees, is mainly based on the use of acaricides. However, more environmentally safe measures, such as biological control, are being encouraged. Life-history traits of the three most abundant phytoseiid mites associated with T. urticae on this crop (Euseius stipulatus, Phytoseiulus persimilis and Neoseiulus californicus) were studied. The experiments were performed under laboratory conditions (25°C, 80 ± 5% RH and 16:8 h (L:D)) on clementine leaves and T. urticae as prey. Euseius stipulatus could not complete its life cycle, whereas P. persimilis and N. californicus completed it satisfactorily. The estimated intrinsic rate of increase (r _m) was significantly higher for P. persimilis (0.344 day⁻¹) than for N. californicus (0.244 day⁻¹) and both were higher than the r _m value of T. urticae on clementine leaves. Implications of these results for the biological control of T. urticae in this crop are discussed.     

Effect of pollen provision on life-history parameters of phytoseiid predators under hot and dry environmental conditions

Biological control can be severely disrupted under climate change conditions. This is the case of the spider mite Tetranychus urticae in Spanish citrus orchards, where the omnivorous phytoseiid Euseius stipulatus, the most abundant predator in the system, was highly impacted by hot and dry conditions mimicking future warmer summers. Such a situation can often be compensated by the provision of alternative food to support generalist predators. As a first step to studying whether such a technique could be applied in this case, we studied at laboratory conditions whether pollen could mitigate the negative effects of hotter and drier conditions derived of climate change on three phytoseiids with different diet specializations. In addition to E. stipulatus, these predators, which all together, are considered key for the biological control of T. urticae in citrus, are Neoseiulus californicus and Phytoseiulus persimilis. Our results confirm the extremely fine-tuning of T. urticae to hot–dry conditions. They also provide evidence of the poor performance of E. stipulatus, especially in terms of reproduction, compared to the other two phytoseiids at these conditions, even when high-quality pollen was available. Moreover, access to pollen in combination with T. urticae eggs enhanced survival but reduced predation and oviposition relative to a T. urticae-only diet for N. californicus and P. persimilis. Therefore, whether the overall effect of pollen would justify its use in citrus to counteract the deleterious effects of a hotter and drier climate on the natural regulation of T. urticae is still controversial.     

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

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

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.     

Disentangling mite predator‐prey relationships by multiplex PCR

Gut content analysis using molecular techniques can help elucidate predator‐prey relationships in situations in which other methodologies are not feasible, such as in the case of trophic interactions between minute species such as mites. We designed species‐specific primers for a mite community occurring in Spanish citrus orchards comprising two herbivores, the Tetranychidae Tetranychus urticae and Panonychus citri, and six predatory mites belonging to the Phytoseiidae family; these predatory mites are considered to be these herbivores’ main biological control agents. These primers were successfully multiplexed in a single PCR to test the range of predators feeding on each of the two prey species. We estimated prey DNA detectability success over time (DS₅₀), which depended on the predator‐prey combination and ranged from 0.2 to 18 h. These values were further used to weight prey detection in field samples to disentangle the predatory role played by the most abundant predators (i.e. Euseius stipulatus and Phytoseiulus persimilis). The corrected predation value for E. stipulatus was significantly higher than for P. persimilis. However, because this 1.5‐fold difference was less than that observed regarding their sevenfold difference in abundance, we conclude that P. persimilis is the most effective predator in the system; it preyed on tetranychids almost five times more frequently than E. stipulatus did. The present results demonstrate that molecular tools are appropriate to unravel predator‐prey interactions in tiny species such as mites, which include important agricultural pests and their predators.     

Ecobiology of Anaphothrips obscurus,a new dweller of citrus orchards brought in by more sustainable pest management practices

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Phenotypic plasticity in anti-intraguild predator strategies: mite larvae adjust their behaviours according to vulnerability and predation risk

Interspecific threat-sensitivity allows prey to maximize the net benefit of antipredator strategies by adjusting the type and intensity of their response to the level of predation risk. This is well documented for classical prey-predator interactions but less so for intraguild predation (IGP). We examined threat-sensitivity in antipredator behaviour of larvae in a predatory mite guild sharing spider mites as prey. The guild consisted of the highly vulnerable intraguild (IG) prey and weak IG predator Phytoseiulus persimilis, the moderately vulnerable IG prey and moderate IG predator Neoseiulus californicus and the little vulnerable IG prey and strong IG predator Amblyseius andersoni. We videotaped the behaviour of the IG prey larvae of the three species in presence of either a low- or a high-risk IG predator female or predator absence and analysed time, distance, path shape and interaction parameters of predators and prey. The least vulnerable IG prey A. andersoni was insensitive to differing IGP risks but the moderately vulnerable IG prey N. californicus and the highly vulnerable IG prey P. persimilis responded in a threat-sensitive manner. Predator presence triggered threat-sensitive behavioural changes in one out of ten measured traits in N. californicus larvae but in four traits in P. persimilis larvae. Low-risk IG predator presence induced a typical escape response in P. persimilis larvae, whereas they reduced their activity in the high-risk IG predator presence. We argue that interspecific threat-sensitivity may promote co-existence of IG predators and IG prey and should be common in predator guilds with long co-evolutionary history.     

Intraguild Predation and Feeding Preferences in Three Species of Phytoseiid Mite Used for Biological Control

The ecological impact of introduced biological control agents on native species of arthropods is a matter of considerable debate. This study investigated the ability of the non-native predatory mite Neoseiulus californicus to feed on the native Typhlodromus pyri and vice versa, as both species now co-occur in UK orchards. Typhlodromips montdorensis is a candidate for introduction into the UK as a glasshouse biological control agent. The ability of T. montdorensis to feed on the widely used N. californicus was investigated to identify possible intraguild predation, which might influence the effectiveness of either or both species as predators of Tetranychus urticae. Both N. californicus and T. pyri consumed larval stages of each other, but in choice experiments both showed a preference for T. urticae. Both N. californicus and T. montdorensis also fed on each other, but whereas N. californicus again showed a preference for T. urticae, T. montdorensis fed equally on T. urticae and N. californicus. Interactions between N. californicus and T. pyri and N. californicus and T. montdorensis are discussed in relation to their effectiveness as biological control agents in the glasshouse and the natural control of spider mite in the field.     

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.     

A New Finding of a the Predatory Mite,Amblyseius californicus (Acari: Phytoseiidae) in Jeju,Korea

Predatory mites in the Family of Phytoseiidae (Acari) are important components in mite biological control. Until now, a native predatory mite, Amblyseius womersleyi has been a subject of intensive studies for implementation of spider mite biological control in fruit orchards, while imported Phytoseiulus persimilis has been successfully implemented in greenhouse environments since 2002. Because of some ecological constraints of A. womersleyi as well as the field environments, spider mite biological control by A. womersleyi has not been successfully implemented. Therefore, demands for another feasible mite predator have increased. This paper reports a newly found predatory mite, Amblyseius californicus, known also as Neosiulus californicus from Jeju citrus orchards. This is the first record of field occurrence of this species in Korea. Some ecological characteristics of this species useful for biological control are also discussed.     

Differential effects of abiotic conditions on fitness-related parameters of two <Emphasis Type="Italic">Euseius</Emphasis> species inhabiting avocado agro-ecosystems

Temperature and relative humidity are important factors in shaping the structure and dynamics of communities composed of ectothermic species, as they directly affect fitness-related parameters and biotic interactions. In a climate change context, increased warming and dryness will likely affect arthropod communities of agro-ecosystems managed by biological pest control. In this work, we compare, at the individual level, the functional relation between temperature and relative humidity and different life-history parameters in two sister predatory mite species that inhabit Spanish avocado crops, Euseius stipulatus and E. scutalis (Athias-Henriot) (Acari: Phytoseiidae). We found that negative effects of high temperature and low relative humidity were stronger in E. stipulatus than in E. scutalis. That E. scutalis tolerates very well hot and dry environments makes the species a good candidate to be considered in the future as a biocontrol agent against pests in subtropical and Mediterranean orchards.     

Effects of predator-mediated apparent competition on the population dynamics of Tetranychus urticae on apples

The two spotted spider mite, Tetranychus urticae Koch, is an important herbivore pest of apple trees in Northwest China. This spider mite and another less damaging spider mite, Eotetranychus pruni Oudemans, are attacked by a common and often effective phytoseiid predator, Euseius finlandicus (Oudemans). Functional relationships were studied in the field to evaluate the impact of E. pruni and E. finlandicus on T. urticae. The results from this study showed that the predator-mediated apparent competition strongly affected the population dynamics of T. urticae. The addition of the apparent competitor E. pruni alone had little impact on T. urticae densities. Although the release of the predator E. finlandicus alone could result in reduction in T. urticae densities, the greatest reduction in T. urticae densities occurred in plots where both the predator E. finlandicus and apparent competitor E. pruni were released. In apple orchards, the early introduction of both the apparent competitor E. pruni and predator E. finlandicus would evidently increase the population size of the predator E. finlandicus and consequently significantly enhance the control of T. urticae populations. It is concluded from the study that the predator and apparent competitor release might be an appropriate control for the target species.     

Population dynamics of interacting predatory mites,Phytoseiulus persimilis and Neoseiulus californicus,held on detached bean leaves

The success of combined release of the predatory mitesPhytoseiulus persimilis and Neoseiulus californicus insuppression of spider mites may be related to the effects of the interactionsbetween the two predators on their population dynamics. We studied populationgrowth and persistence of the specialist P. persimilis andthe generalist N. californicus reared singly versus rearedin combination after simultaneous and successive predator introductions ondetached bean leaf arenas with abundant prey, Tetranychusurticae, and with diminishing prey. When reared singly with abundantprey, either predator population persisted at high densities to the end of theexperiment. In every predator combination system with abundant prey and variousinitial predator:predator ratios N. californicus displacedP. persimilis. When held singly with diminishing prey, thepopulation of P. persimilis grew initially faster than thepopulation of N. californicus but both species reachedsimilar population peaks. Irrespective whether reared singly or in combination,N. californicus persisted three to five times longer afterprey depletion than did P. persimilis. Regarding thecrucial interactions in the predator combination systems, we conclude thatintraguild predation was a stronger force than food competition and finallyresulted in the displacement of P. persimilis. Previousstudies showed that intraguild predation between the specialist P.persimilis and the generalist N. californicusisstrongly asymmetric favoring the generalist. We discuss the implications ofpotential interactions between P. persimilis andN. californicus to biological control of spider mites.     

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.     

Interactions among phytophagous mites, and introduced and naturally occurring predatory mites, on strawberry in the UK

In choice test experiments on strawberry leaf disc arenas the phytoseiid mites Neoseiulus californicus and N. cucumeris were more effective than Typhlodromus pyri as predators of the phytophagous mites Tetranychus urticae and Phytonemus pallidus. There were no preferences shown for either prey by any of these predators. In multiple predator leaf disc experiments both Phytoseiulus persimilis and N. cucumeris significantly reduced numbers of T. urticae eggs and active stages; this effect was seen when the two species were present alone or in combination with other predator species. Neoseiulus californicus was less effective at reducing T. urticae numbers, and T. pyri was not effective; no interaction between predator species was detected in these experiments. When T. urticae alone was present as prey on potted plants, P. persimilis and N. californicus were the only phytoseiids to significantly reduce T. urticae numbers. These two predator species provided effective control of T. urticae when P. pallidus was also present; however, none of the predators reduced numbers of P. pallidus. There were no significant negative interactions when different species of predators were present together on these potted plants. In field experiments, releases of both P. persimilis and N. cucumeris significantly reduced T. urticae numbers. However, there was a significant interaction between these predator species, leading to poorer control of T. urticae when both species were released together. These results show the importance of conducting predator/prey feeding tests at different spatial scales.     

Multiple indole glucosinolates and myrosinases defend Arabidopsis against Tetranychus urticae herbivory

Arabidopsis (Arabidopsis thaliana) defenses against herbivores are regulated by the jasmonate (JA) hormonal signaling pathway, which leads to the production of a plethora of defense compounds. Arabidopsis defense compounds include tryptophan-derived metabolites, which limit Arabidopsis infestation by the generalist herbivore two-spotted spider mite, Tetranychus urticae. However, the phytochemicals responsible for Arabidopsis protection against T. urticae are unknown. Here, we used Arabidopsis mutants disrupted in the synthesis of tryptophan-derived secondary metabolites to identify phytochemicals involved in the defense against T. urticae. We show that of the three tryptophan-dependent pathways found in Arabidopsis, the indole glucosinolate (IG) pathway is necessary and sufficient to assure tryptophan-mediated defense against T. urticae. We demonstrate that all three IGs can limit T. urticae herbivory, but that they must be processed by myrosinases to hinder T. urticae oviposition. Putative IG breakdown products were detected in mite-infested leaves, suggesting in planta processing by myrosinases. Finally, we demonstrate that besides IGs, there are additional JA-regulated defenses that control T. urticae herbivory. Together, our results reveal the complexity of Arabidopsis defenses against T. urticae that rely on multiple IGs, specific myrosinases, and additional JA-dependent defenses.

Three IGs and specific myrosinases help protect Arabidopsis thaliana against herbivory by the two-spotted spider mite T. urticae.     

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.     

Influence of food and temperature on development and oviposition ofEuseius stipulatus andTyphlodromus phialatus (Acari: Phytoseiidae)

The influence of feeding and temperature on life table parameters ofEuseius stipulatus (Athias-Henriot) andTyphlodromus phialatus Athias-Henriot was determined in laboratory tests. Both phytoseiids developed and reproduced readily when fed onCarpobrotus edulis (L.) pollen andPanonychus citri (McGregor) Intrinsic rates of increase (r _m ) at 25°C forE. stipulatus andT. phialatus were 0.197 and 0.126, and, when fed onP. citri, 0.129 and 0.144, respectively.Tetranychus urticae Koch offered as prey allowed normal development and oviposition ofT. phialatus, but no eggs were laid byE. stipulatus when fed on this spider mite. Eggs and honeydew ofAleurothrixus floccosus Mask. furnished sufficient nutrition for development of immatures ofE. stipulatus. Larvae ofPlanoccocus citri Risso, and honeydew and eggs ofA. floccosus, allowed adult survival but no egg-laying of the predaceous mites.Lorryia formosa Cooreman was not a favoured prey species.Life tables were calculated forE. stipulatus fed on pollen andT. phialatus fed onP. citri at constant temperatures of 18, 25, and 32°C. Maximum development was reached at 32°C, withr _m values of 0.225 forE. stipulatus and 0.179 forT. phialatus. In general, both phytoseiids showed medium to high total number of eggs per female and long oviposition periods when compared with other phytoseiid species.When mating took place at 32°C,E. stipulatus females were not able to lay eggs, thus suggesting an interference of high temperatures with fertilization in this species. No hatching was observed in eggs of either species when kept at relative humidities of 50% or lower. The possible significance of these responses is discussed in relation to population trends observed in the field.