Summary1. Indirect induced plant defence via emission of herbivore-induced plant volatiles (HIPV) to recruit natural enemies of herbivores is a ubiquitous phenomenon, but whether and how emission of above-ground HIPVs is adaptively modulated by below-ground mutualistic microorganisms is unknown. 2. We investigated the effects of the mycorrhizal fungus Glomus mosseae on chemical composition of HIPVs emitted by bean plants Phaseolus vulgaris attacked by spider mites, Tetranychus urticae, using proton-transfer mass spectrometry, and attraction of the spider mites' natural enemy, the predatory mite Phytoseiulus persimilis, to these HIPVs using a Y-tube olfactometer. 3. Mycorrhiza significantly changed the HIPV composition. Most notably, it increased the emission of b-ocimene and b-caryophyllene, two compounds synthesized de novo upon spider mite attack. The constitutively emitted methyl salicylate was increased by spider mite infestation but decreased by mycorrhiza. 4. The predators responded strongly to HIPVs emitted by plants infested for 6 days and preferred HIPVs of mycorrhizal plants to those of non-mycorrhizal plants. In contrast, they were less responsive and indiscriminative to mycorrhization when exposed to volatiles emitted by non-infested plants and plants infested by spider mites for 1 or 3 days. 5. Our study provides a key example of an adaptive indirect HIPV-mediated interaction of a below-ground micro-organism with an above-ground carnivore.

1. Arbuscular mycorrhiza (AM), the association of AM fungi and plant roots, may alter morphological and physiological attributes of aboveground plant parts and thereby influence plant-associated organisms such as herbivores and their natural enemies, predators and parasitoids.2. The interactions between AM and the players of aboveground tri-trophic systems have mainly been considered in isolation from each other. The effects of AM on aboveground herbivore-carnivore population dynamics and the consequences to plant fitness are unknown.3. We explored AM-induced compensatory mechanisms for AM-promoted proliferation of the herbivorous spider mite, Tetranychus urticae Koch, on whole bean plants, Phaseolus vulgaris L. Vegetative and reproductive plant growth, AM fungal colonisation levels, and mite densities were assessed on spider mite-infested plants colonised or not by the AM fungus Glomus mosseae Nicol. & Gerd, and harbouring the natural enemy of the spider mites, the predatory mite Phytoseiulus persimilis Anthias-Henriot or not.4. AM symbiosis modulated the aboveground tri-trophic system to the fitness benefit of the plant. AM-increased plant productivity outweighed the fitness decrease due to AM-promoted herbivory: at similar vegetative growth, mycorrhizal plants produced more seeds than non-mycorrhizal plants.5. AM-increased spider mite population levels were compensated for by enhanced population growth of the predators and increased plant tolerance to herbivory.6. AM-enhanced predator performance looped back to the AM fungus and stabilised its root colonisation levels, providing the first experimental evidence of a mutually beneficial interaction between AM and an aboveground third trophic level natural enemy.

BackgroundLearning processes can be broadly categorized into associative and non-associative. Associative learning occurs through the pairing of two previously unrelated stimuli, whereas non-associative learning occurs in response to a single stimulus. How these two principal processes compare in the same learning task and how they contribute to the overall behavioural changes brought about by experience is poorly understood. We tackled this issue by scrutinizing associative and non-associative learning of prey, Western flower thrips Frankliniella occidentalis, by the predatory mite, Neoseiulus californicus. We compared the behaviour of thrips-experienced and -naïve predators, which, early in life, were exposed to either thrips with feeding (associative learning), thrips without feeding (non-associative learning), thrips traces on the surface (non-associative learning), spider mites with feeding (thrips-naïve) or spider mite traces on the surface (thrips-naïve).ResultsThrips experience in early life, no matter whether associative or not, resulted in higher predation rates on thrips by adult females. In the no-choice experiment, associative thrips experience increased the predation rate on the first day, but shortened the longevity of food-stressed predators, a cost of learning. In the choice experiment, thrips experience, no matter whether associative or not, increased egg production, an adaptive benefit of learning.ConclusionsOur study shows that both non-associative and associative learning forms operate in foraging predatory mites, N. californicus. The non-rewarded thrips prey experience produced a slightly weaker, but less costly, learning effect than the rewarded experience. We argue that in foraging predatory mites non-associative learning is an inevitable component of associative learning, rather than a separate process.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-016-0112-x) contains supplementary material, which is available to authorized users.

BackgroundIn group-living animals, social interactions and their effects on other life activities such as foraging are commonly determined by discrimination among group members. Accordingly, many group-living species evolved sophisticated social recognition abilities such as the ability to recognize familiar individuals, i.e. individuals encountered before. Social familiarity may affect within-group interactions and between-group movements. In environments with patchily distributed prey, group-living predators must repeatedly decide whether to stay with the group in a given prey patch or to leave and search for new prey patches and groups.Methodology/Principal FindingsBased on the assumption that in group-living animals social familiarity allows to optimize the performance in other tasks, as for example predicted by limited attention theory, we assessed the influence of social familiarity on prey patch exploitation, patch-leaving, and inter-patch distribution of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. P. persimilis is highly specialized on herbivorous spider mite prey such as the two-spotted spider mite Tetranychus urticae, which is patchily distributed on its host plants. We conducted two experiments with (1) groups of juvenile P. persimilis under limited food on interconnected detached leaflets, and (2) groups of adult P. persimilis females under limited food on whole plants. Familiar individuals of both juvenile and adult predator groups were more exploratory and dispersed earlier from a given spider mite patch, occupied more leaves and depleted prey more quickly than individuals of unfamiliar groups. Moreover, familiar juvenile predators had higher survival chances than unfamiliar juveniles.Conclusions/SignificanceWe argue that patch-exploitation and -leaving, and inter-patch dispersion were more favorably coordinated in groups of familiar than unfamiliar predators, alleviating intraspecific competition and improving prey utilization and suppression.

Bioassays using bean leaf discs were conducted to investigate toxic and behaviour-modifying effects of carvacrol and thymol, two monoterpenoid phenols, on second instar larvae of Frankliniella occidentalis (Thysanoptera: Thripidae) at concentrations of 0.1% and 1%. We tested the contact toxicity of carvacrol and thymol to F. occidentalis larvae and studied the settlement preference of thrips larvae for treated or untreated bean leaf discs and the effects of the compounds on their feeding activity. Mortality rates after 24 h were 24.1% for carvacrol at 1% concentration, 16.5% for carvacrol at 0.1%, 7.7% for thymol at 1% concentration and 3.6% for thymol at 0.1%. Thrips larvae showed a significant preference for untreated leaf discs in choice tests with carvacrol 1% or thymol 1%. Likewise, in the no-choice tests feeding damage after 24 h was significantly lower on leaf discs treated with 1% carvacrol or 1% thymol compared to the control, but not on discs treated with 0.1% concentration of either compound. We conclude that an application of carvacrol or thymol to bean leaves does not result in a high mortality of F. occidentalis larvae but affects their behaviour.