BackgroundPlants have inducible defenses to combat attacking organisms. Hence, some herbivores have adapted to suppress these defenses. Suppression of plant defenses has been shown to benefit herbivores by boosting their growth and reproductive performance.ResultsWe observed in field-grown tomatoes that spider mites (Tetranychus urticae) establish larger colonies on plants already infested with the tomato russet mite (Aculops lycopersici). Using laboratory assays, we observed that spider mites have a much higher reproductive performance on russet mite-infested plants, similar to their performance on the jasmonic acid (JA)-biosynthesis mutant def-1. Hence, we tested if russet mites suppress JA-responses thereby facilitating spider mites. We found that russet mites manipulate defenses: they induce those mediated by salicylic acid (SA) but suppress those mediated by JA which would otherwise hinder growth. This suppression of JA-defenses occurs downstream of JA-accumulation and is independent from its natural antagonist SA. In contrast, spider mites induced both JA- and SA-responses while plants infested with the two mite species together display strongly reduced JA-responses, yet a doubled SA-response. The spider mite-induced JA-response in the presence of russet mites was restored on transgenic tomatoes unable to accumulate SA (nahG), but russet mites alone still did not induce JA-responses on nahG plants. Thus, indirect facilitation of spider mites by russet mites depends on the antagonistic action of SA on JA while suppression of JA-defenses by russet mites does not. Furthermore, russet mite-induced SA-responses inhibited secondary infection by Pseudomonas syringae (Pst) while not affecting the mite itself. Finally, while facilitating spider mites, russet mites experience reduced population growth.ConclusionsOur results show that the benefits of suppressing plant defenses may diminish within communities with natural competitors. We show that suppression of defenses via the JA-SA antagonism can be a consequence, rather than the cause, of a primary suppression event and that its overall effect is determined by the presence of competing herbivores and the distinct palette of defenses these induce. Thus, whether or not host-defense manipulation improves an herbivore’s fitness depends on interactions with other herbivores via induced-host defenses, implicating bidirectional causation of community structure of herbivores sharing a plant.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0098-9) contains supplementary material, which is available to authorized users.

Tomato plants have their leaves, petioles and stems covered with glandular trichomes that protect the plant against two-spotted spider mites and many other herbivorous arthropods, but also hinder searching by phytoseiid mites and other natural enemies of these herbivores. This trichome cover creates competitor-free and enemy-free space for the tomato russet mite (TRM) Aculops lycopersici (Acari: Eriophyidae), being so minute that it can seek refuge and feed inbetween the glandular trichomes on tomato cultivars currently used in practice. Indeed, several species of predatory mites tested for biological control of TRM have been reported to feed and reproduce when offered TRM as prey in laboratory experiments, yet in practice these predator species appeared to be unable to prevent TRM outbreaks. Using the phytoseiid mite, Amblydromalus limonicus, we found exactly the same, but also obtained evidence for successful establishment of a population of this predatory mite on whole plants that had been previously infested with TRM. This successful establishment may be explained by our observation that the defensive barrier of glandular plant trichomes is literally dropped some time after TRM infestation of the tomato plants: the glandular trichome heads first rapidly develop a brownish discoloration after which they dry out and fall over onto the plant surface. Wherever TRM triggered this response, predatory mites were able to successfully establish a population. Nevertheless, biological control was still unsuccessful because trichome deterioration in TRM-infested areas takes a couple of days to take effect and because it is not a systemic response in the plant, thereby enabling TRM to seek temporary refuge from predation in pest-free trichome-dense areas which continue to be formed while the plant grows. We formulate a hypothesis unifying these observations into one framework with an explicit set of assumptions and predictions to be tested in future experiments.Electronic supplementary materialThe online version of this article (doi:10.1007/s10493-012-9638-6) contains supplementary material, which is available to authorized users.

The nature of the damage caused by eriophyoid mites and the assessment of yield losses still require detailed studies if appropriate control and risk mitigation strategies are to be planned. The economic importance of eriophyoid mites is increasing worldwide and a lot of species have reached a permanent pest status in certain crops, while others represent a quarantine threat for several countries. Due to their relevant role in Europe and elsewhere, three eriophyoid mites that have been frequently reported in recent research, are here considered as case studies: two of them (the apple rust mite, Aculus schlechtendali, and the grape rust mite, Calepitrimerus vitis) colonise temperate fruits, while one (the tomato russet mite, Aculops lycopersici) affects vegetables. The damage assessment related to the apple rust mite has been evaluated on different apple varieties with implications for pest control. Some factors affecting the spread and economic importance of the grape rust mite have been identified. The complexity and difficulty in controlling the tomato russet mite by chemicals enhances the interest in biological control agents. Considerations on interactions between eriophyoids and host plants (e.g. resistance, varietal susceptibility), on pest management regimes (e.g. impact of fungicides, resistance to acaricides, perspectives on biological control) are presented.

BackgroundPlants have inducible defenses to combat attacking organisms. Hence, some herbivores have adapted to suppress these defenses. Suppression of plant defenses has been shown to benefit herbivores by boosting their growth and reproductive performance.ResultsWe observed in field-grown tomatoes that spider mites (Tetranychus urticae) establish larger colonies on plants already infested with the tomato russet mite (Aculops lycopersici). Using laboratory assays, we observed that spider mites have a much higher reproductive performance on russet mite-infested plants, similar to their performance on the jasmonic acid (JA)-biosynthesis mutant def-1. Hence, we tested if russet mites suppress JA-responses thereby facilitating spider mites. We found that russet mites manipulate defenses: they induce those mediated by salicylic acid (SA) but suppress those mediated by JA which would otherwise hinder growth. This suppression of JA-defenses occurs downstream of JA-accumulation and is independent from its natural antagonist SA. In contrast, spider mites induced both JA- and SA-responses while plants infested with the two mite species together display strongly reduced JA-responses, yet a doubled SA-response. The spider mite-induced JA-response in the presence of russet mites was restored on transgenic tomatoes unable to accumulate SA (nahG), but russet mites alone still did not induce JA-responses on nahG plants. Thus, indirect facilitation of spider mites by russet mites depends on the antagonistic action of SA on JA while suppression of JA-defenses by russet mites does not. Furthermore, russet mite-induced SA-responses inhibited secondary infection by Pseudomonas syringae (Pst) while not affecting the mite itself. Finally, while facilitating spider mites, russet mites experience reduced population growth.ConclusionsOur results show that the benefits of suppressing plant defenses may diminish within communities with natural competitors. We show that suppression of defenses via the JA-SA antagonism can be a consequence, rather than the cause, of a primary suppression event and that its overall effect is determined by the presence of competing herbivores and the distinct palette of defenses these induce. Thus, whether or not host-defense manipulation improves an herbivore’s fitness depends on interactions with other herbivores via induced-host defenses, implicating bidirectional causation of community structure of herbivores sharing a plant.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0098-9) contains supplementary material, which is available to authorized users.

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