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Phytoseiulus longipes is a predatory mite of Tetranychus evansi, which is an invasive pest in Africa and elsewhere. The introduction of this predator in Africa has considerable potential, but little is known about the compatibility of P. longipes with commonly used pesticides. Here, we examined lethal and sublethal effects of two pyrethroids (cypermethrin and deltamethrin), two organophosphates (dimethoate and chlorpyrifos), one nicotinoid (imidacloprid), two acaricides (propargite and abamectin), two naturally derived pesticides (oxymatrine and azadirachtin), and one entomopathogenic fungal-based formulation (Hirsutella thompsonii) on P. longipes eggs and adults. The pesticides were sprayed at their maximum recommended concentrations. Topical exposures to azadirachtin, imidacloprid, propargite, abamectin, oxymatrine, and H. thompsonii significantly reduced the net reproductive rate (R0), intrinsic rate of increase (r) and finite rate of increase (λ)of P. longipes. Pesticide lethal and sublethal effects on the predator were summarized in a reduction coefficient (Ex) for the classification based on IOBC toxicity categories. Results revealed that Azadirachtin and H. thompsonii were slightly harmful effects to adults. Imidacloprid, propargite, abamectin, and oxymatrine were moderately harmful to both eggs and adults. Residual persistence bioassays revealed that 4-day-old residue of azadirachtin had no harmful effect on the predator. Abamectin, oxymatrine, and H. thompsonii became harmless to it 10 days post-spraying, and propargite and imidacloprid were considered harmless after 20 days. Cypermethrin, deltamethrin, dimethoate, and chlorpyrifos were highly harmful to both eggs and adults, persistence remaining high even after 31 days of application. These findings provide valuable insights into decision-making when considering P. longipes for use in IPM programs.

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Metal accumulation is used by some plants as a defence against herbivores. Yet, herbivores may adapt to these defences, becoming less susceptible. Moreover, ecosystems often contain plants that do and do not accumulate metals, but whether such heterogeneity affects herbivore adaptation remains understudied. Here, we performed experimental evolution to test whether the spider mite Tetranychus evansi adapts to plants with high cadmium concentrations, in homogeneous (plants with cadmium) or heterogeneous (plants with or without cadmium) environments. For that we used tomato plants, which accumulate cadmium, thus affecting the performance of these spider mites. We measured mite fecundity, hatching rate, and the number of adult offspring after 12 and 33 generations and habitat choice after 14 and 51 generations, detecting no trait change, which implies the absence of adaptation. We then tested whether this was due to a lack of genetic variation in the traits measured and, indeed, additive genetic variance was low. Interestingly, despite no signs of adaptation, we observed a decrease in fecundity and number of adult offspring produced on cadmium-free plants, in the populations evolving in environments with cadmium. Therefore, evolving in environments with cadmium reduces the growth rate of spider mite populations on non-accumulating plants. Possibly, other traits contributed to population persistence on plants with cadmium. This calls for more studies addressing herbivore adaptation to plant metal accumulation.

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Herbivore-associated elicitors (HAEs) are active molecules produced by herbivorous insects. Recognition of HAEs by plants induces defence that resist herbivore attacks. We previously demonstrated that the tomato red spider mite Tetranychus evansi triggered defence in Nicotiana benthamiana. However, our knowledge of HAEs from T. evansi remains limited. Here, we characterize a novel HAE, Te16, from T. evansi and dissect its function in mite-plant interactions. We investigate the effects of Te16 on spider mites and plants by heterologous expression, virus-induced gene silencing assay, and RNA interference. Te16 induces cell death, reactive oxygen species (ROS) accumulation, callose deposition, and jasmonate (JA)-related responses in N. benthamiana leaves. Te16-mediated cell death requires a calcium signalling pathway, cytoplasmic localization, the plant co-receptor BAK1, and the signalling components SGT1 and HSP90. The active region of Te16-induced cell death is located at amino acids 114-293. Moreover, silencing Te16 gene in T. evansi reduces spider mite survival and hatchability, but expressing Te16 in N. benthamiana leaves enhances plant resistance to herbivores. Finally, Te16 gene is specific to Tetranychidae species and is highly conserved in activating plant immunity. Our findings reveal a novel salivary protein produced by spider mites that elicits plant defence and resistance to insects, providing valuable clues for pest management.

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Two mutually unexclusive hypotheses prevail in the theory of nutritional ecology: the balanced diet hypothesis states that consumers feed on different food items because they have complementary nutrient and energy compositions. The toxin-dilution hypothesis poses that consumers feed on different food items to dilute the toxins present in each. Both predict that consumers should not feed on low-quality food when ample high-quality food forming a complete diet is present. We investigated the diet choice of Phytoseiulus persimilis, a predatory mite of web-producing spider mites. It can develop and reproduce on single prey species, for example the spider mite Tetranychus urticae. A closely related prey, T. evansi, is of notorious bad quality for P. persimilis and other predator species. We show that juvenile predators feeding on this prey have low survival and do not develop into adults. Adults stop reproducing and have increased mortality when feeding on it. Feeding on a mixed diet of the two prey decreases predator performance, but short-term effects of feeding on the low-quality prey can be partially reversed by subsequently feeding on the high-quality prey. Yet, predators consume low-quality prey in the presence of high-quality prey, which is in disagreement with both hypotheses. We suggest that it is perhaps not the instantaneous reproduction on single prey or mixtures of prey that matters for the fitness of predators, but that it is the overall reproduction by a female and her offspring on an ephemeral prey patch, which may be increased by including inferior prey in their diet.

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Spider mites (Tetranychidae) are destructive agricultural pests which have evolved strategies to overcome plant defenses, such as the ability to puncture the leaves of their hosts to feed. The expression of many genes with unknown functions is altered during feeding, but little is known about the role of these genes in plant-mite interactions. Here, we identified 3 novel gene families through analysis of genomic and transcriptomic data from 3 spider mite species. These GARP family genes encode glycine and alanine-rich proteins; they are present in mites (Acariformes) but absent in ticks (Parasitiformes) in the subclass Acari, indicating that these genes have undergone a significant expansion in spider mites and thus play important adaptive roles. Transcriptomic analysis revealed that the expression of GARP genes is strongly correlated with feeding and the transfer to new hosts. We used RNA interference to silence GARP1d in the two-spotted spider mite Tetranychus urticae, which inhibited feeding and egg laying and significantly increased mortality when the mites were transferred to soybean shoots; a similar effect was observed after TuVATPase was silenced. However, no changes in mite mortality were observed after TuGARP1d-silenced mites were placed on an artificial diet, which was different from the effect of TuVATPase silencing. Our results indicate that GARP family members play important roles in mite-plant interactions. Additional studies are needed to clarify the mechanisms underlying these interactions.

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Competitive interaction between sister species can be affected by reproductive interference (RI) depending on the ability of males to discriminate conspecific from heterospecific mates. We study such interactions in Tetranychus evansi and T. urticae. These spider mites co-occur on solanaceous plants in Southern Europe, and cause important yield losses in tomato crops. Previous studies using Spanish populations found that T. evansi outcompetes T. urticae, and that this is due to unidirectional RI of T. evansi males with T. urticae females. The unidirectional RI is attributed to differences in male mate preference for conspecific females between the two species. Also, differences in the propensity of interspecific web sharing in females plays a role. To investigate proximate mechanisms of this RI, here we study the role of female pheromones on male mate preference and female web sharing. We extracted pheromones from females of the two species, and investigated if males and females were arrested by the pheromone extractions in various concentrations. We observed that T. urticae males were more sensitive to the pheromone extractions and able to discriminate conspecific from heterospecific ones. Tetranychus evansi males, on the other hand, were less sensitive. Females from both species were arrested by conspecific pheromone extraction in lower concentrations. In conclusion, heterospecific mating by T. evansi males, which results in RI, can be explained by their lack of discrimination between female pheromones of the two species. Differences in the propensity of interspecific web sharing in females might not be explained by the pheromones that we investigated.

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The spider mite Tetranychus evansi has a remarkable ability to suppress and manipulate plant defenses, which makes it an ideal model to investigate plant-herbivores interactions. In this study, a de novo assembly of the transcriptome of T. evansi is performed and the proteins in its secreted saliva by LC-MS/MS are characterized. A total of 29 365 unigenes are assembled and 136 saliva proteins are identified. Comparative analysis of the saliva proteins in T. evansi, T. truncatus, and T. urticae shows that 64 protein groups are shared by at least two Tetranychus species, and 52 protein groups are specifically identified in T. evansi. In addition, some saliva proteins are common in arthropod species, while others are species-specific. These results will help to elucidate the molecular mechanisms by which T. evansi modulates plant defenses.

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It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores. Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied. We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses. Plant quality was quantified through oviposition of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species. Spider-mite oviposition data show that T. evansi could suppress an earlier induction of plant defenses by T. urticae, and T. urticae could induce defenses in plants previously attacked by T. evansi in 1 day. Longer attacks by the second species did not result in further changes in oviposition. Proteinase inhibitor activity levels showed that T. evansi suppressed the high activity levels induced by T. urticae to constitutive levels in 1 day, and further suppressed activity to levels similar to those in plants attacked by T. evansi alone. Attacks by T. urticae induced proteinase inhibitor activity in plants previously attacked by T. evansi, eventually to similar levels as induced by T. urticae alone. Hence, plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance, but does affect proteinase inhibitor activity levels. Based on our results, we discuss the evolution of suppression of plant defenses.

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BACKGROUND: Tetranychus evansi and T. urticae spider mites are known major pests of Solanaceae. Smallholders in Africa rely heavily on pesticide treatments. However, farmers claim that pesticides are generally ineffective despite high-frequency sprays. New management solutions are thus urgently needed. This study assessed the efficacy of using acaricide-treated nets combined with predatory mite release for controlling spider mites. RESULTS: The results showed the acaricide-treated net alone was more effective at reducing numbers of T. urticae than T. evansi. We observed the opposite for release of the predatory mite Phytoseiulus longipes. This difference could be explained by the specific dispersion strategies of the two spider mite pests; T. evansi is gregarious, whereas T. urticae dispersed rapidly. Joint application of both techniques resulted in a synergetic effect that reduced T. evansi and T. urticae spider mite numbers close to zero. The synergetic effect could be explained by predator avoidance behaviour of the prey spider mites, resulting in higher prey trapping and killing rates on acaricide-treated nets, while P. longipes fed on spider mite eggs. CONCLUSION: These techniques are profitable for smallholders as they are not expensive and avoid residues on the crop. © 2018 Society of Chemical Industry.

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Tomato plants are attacked by diverse herbivorous arthropods, including by cell-content-feeding mites, such as the extreme generalist Tetranychus urticae and specialists like Tetranychus evansi and Aculops lycopersici. Mite feeding induces plant defense responses that reduce mite performance. However, T. evansi and A. lycopersici suppress plant defenses via poorly understood mechanisms and, consequently, maintain a high performance on tomato. On a shared host, T. urticae can be facilitated by either of the specialist mites, likely due to the suppression of plant defenses. To better understand defense suppression and indirect plant-mediated interactions between herbivorous mites, we used gene-expression microarrays to analyze the transcriptomic changes in tomato after attack by either a single mite species (T. urticae, T. evansi, A. lycopersici) or two species simultaneously (T. urticae plus T. evansi or T. urticae plus A. lycopersici). Additionally, we assessed mite-induced changes in defense-associated phytohormones using LC-MS/MS. Compared to non-infested controls, jasmonates (JAs) and salicylate (SA) accumulated to higher amounts upon all mite-infestation treatments, but the response was attenuated after single infestations with defense-suppressors. Strikingly, whereas 8 to 10% of tomato genes were differentially expressed upon single infestations with T. urticae or A. lycopersici, respectively, only 0.1% was altered in T. evansi-infested plants. Transcriptome analysis of dual-infested leaves revealed that A. lycopersici primarily suppressed T. urticae-induced JA defenses, while T. evansi dampened T. urticae-triggered host responses on a transcriptome-wide scale. The latter suggests that T. evansi not solely down-regulates plant gene expression, but rather directs it back towards housekeeping levels. Our results provide valuable new insights into the mechanisms underlying host defense suppression and the plant-mediated facilitation of competing herbivores.

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When feeding from tomato (Solanum lycopersicum), the generalist spider mite Tetranychus urticae induces jasmonate (JA)- and salicylate (SA)-regulated defense responses that hamper its performance. The related T. evansi, a Solanaceae-specialist, suppresses these defenses, thereby upholding a high performance. On a shared leaf, T. urticae can be facilitated by T. evansi, likely via suppression of defenses by the latter. Yet, when infesting the same plant, T. evansi outcompetes T. urticae. Recently, we found that T. evansi intensifies suppression of defenses locally, i.e., at its feeding site, after T. urticae mites were introduced onto adjacent leaf tissue. This hyper-suppression is paralleled by an increased oviposition rate of T. evansi, probably promoting its competitive population growth. Here we present additional data that not only provide insight into the spatiotemporal dynamics of defense induction and suppression by mites, but that also suggest T. evansi to manipulate more than JA and SA defenses alone.

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Spider mites are destructive arthropod pests on many crops. The generalist herbivorous mite Tetranychus urticae induces defenses in tomato (Solanum lycopersicum) and this constrains its fitness. By contrast, the Solanaceae-specialist Tetranychus evansi maintains a high reproductive performance by suppressing tomato defenses. Tetranychus evansi outcompetes T. urticae when infesting the same plant, but it is unknown whether this is facilitated by the defenses of the plant. We assessed the extent to which a secondary infestation by a competitor affects local plant defense responses (phytohormones and defense genes), mite gene expression and mite performance. We observed that T. evansi switches to hyper-suppression of defenses after its tomato host is also invaded by its natural competitor T. urticae. Jasmonate (JA) and salicylate (SA) defenses were suppressed more strongly, albeit only locally at the feeding site of T. evansi, upon introduction of T. urticae to the infested leaflet. The hyper-suppression of defenses coincided with increased expression of T. evansi genes coding for salivary defense-suppressing effector proteins and was paralleled by an increased reproductive performance. Together, these observations suggest that T. evansi overcompensates its reproduction through hyper-suppression of plant defenses in response to nearby competitors. We hypothesize that the competitor-induced overcompensation promotes competitive population growth of T. evansi on tomato.

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Tenuipalpidae comprises mites that transmit viruses to agriculturally important plants. Several tenuipalpid species present parthenogenesis, and in Brevipalpus yothersi, the endosymbiont Cardinium has been associated with female-only colonies. It is unclear what the bacterial composition of B. yothersi is, and how common Cardinium is in those microbiomes. We performed a comparative analysis of the bacteriomes in three populations of B. yothersi and three additional Tetranychoidea species using sequences from V4-fragment of 16S DNA. The bacteriomes were dominated by Bacteroidetes (especially Cardinium) and Proteobacteria, showing a remarkably low alpha diversity. Cardinium was present in about 22% of all sequences; however, it was not present in R. indica and T. evansi. In B. yothersi, the proportion of Cardinium was higher in adults than eggs, suggesting that proliferation of the bacteria could be the result of selective pressures from the host. This hypothesis was further supported because colonies of B. yothersi from different populations showed different bacterial assemblages, and bacteriomes from different mite species showed similar abundances of Cardinium. A phylogenetic analysis of Cardinium revealed that not only specialization but horizontal transmission has been important for this symbiosis. Together, these results represent a glimpse into the evolution of the Tetranychoidea and Cardinium.

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Prey are known to invest in costly antipredator behaviour when perceiving cues of dangerous, but not of relatively harmless predators. Whereas most studies investigate one type of antipredator behaviour, we studied several types (changes in oviposition, in escape and avoidance behaviour) in the spider mite Tetranychus evansi in response to cues from two predatory mites. The predator Phytoseiulus longipes is considered a dangerous predator for T. evansi, whereas Phytoseiulus macropilis has a low predation rate on this prey, thus is a much less dangerous predator. Spider mite females oviposited less on leaf disc halves with predator cues than on clean disc halves, independent of the predator species. On entire leaf discs, they laid fewer eggs in the presence of cues of the dangerous predator than on clean discs, but not in the presence of cues of the harmless predator. Furthermore, the spider mites escaped more often from discs with cues of the dangerous predator than from discs without predator cues, but they did not escape more from discs with cues of the harmless predator. The spider mites did not avoid plants with conspecifics and predators. We conclude that the spider mites displayed several different antipredator responses to the same predator species, and that some of these antipredator responses were stronger with cues of dangerous predators than with cues of harmless predators.

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Spider mites (Tetranychidae sp.) are widely occurring arthropod pests on cultivated plants. Feeding by the two-spotted spider mite T. urticae, a generalist herbivore, induces a defense response in plants that mainly depends on the phytohormones jasmonic acid and salicylic acid (SA). On tomato (Solanum lycopersicum), however, certain genotypes of T. urticae and the specialist species T. evansi were found to suppress these defenses. This phenomenon occurs downstream of phytohormone accumulation via an unknown mechanism. We investigated if spider mites possess effector-like proteins in their saliva that can account for this defense suppression. First we performed an in silico prediction of the T. urticae and the T. evansi secretomes, and subsequently generated a short list of candidate effectors based on additional selection criteria such as life stage-specific expression and salivary gland expression via whole mount in situ hybridization. We picked the top five most promising protein families and then expressed representatives in Nicotiana benthamiana using Agrobacterium tumefaciens transient expression assays to assess their effect on plant defenses. Four proteins from two families suppressed defenses downstream of the phytohormone SA. Furthermore, T. urticae performance on N. benthamiana improved in response to transient expression of three of these proteins and this improvement was similar to that of mites feeding on the tomato SA accumulation mutant nahG. Our results suggest that both generalist and specialist plant-eating mite species are sensitive to SA defenses but secrete proteins via their saliva to reduce the negative effects of these defenses.

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BACKGROUND: Tetranychus evansi is an invasive pest of solanaceous crops in Africa, and in the field it differentially attacks edible African nightshades. The chemical basis for the differential attack on these plant species is largely unknown. Using bioassays and chemical analysis, we investigated the differential bioactivity of leaf extracts of three edible African nightshade species, Solanum sarrachoides, S. scabrum and S. villosum, on adult T. evansi females. RESULTS: Only the bioactivity of the leaf extract of S. sarrachoides (LC50 7.44 mg mL(-1)) and that of its most polar fraction (LC50 5.44 mg mL(-1)) paralleled that of the positive control, neem oil (LC50 1.89 mg mL(-1)), across all doses tested. Liquid chromatography-quadruple time of flight-mass spectrometry identified a mixture of steroidal glycoalkaloids (SGAs), including α-solasonine, α-solamargine and derivatives of tomatine and demissine, which were neither detected in the crude extract nor in any of the fractions obtained from S. scabrum and S. villosum. CONCLUSION: Our results suggest that the presence of SGAs may play a key role in the differential defence of edible African nightshades against attack by T. evansi. These findings may add to the plethora of environmentally friendly tools from natural plant products for management of T. evansi.

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