Mycorrhiza modulates aboveground tri-trophic interactions to the fitness benefit of its host plant

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.