Mycorrhiza-induced trophic cascade enhances fitness and population growth of an acarine predator

Abstract

Research on trophic cascades in terrestrial ecosystems has only recently revealed that root-associated organisms interact with organisms living on aboveground plant parts. Arbuscular mycorrhizal (AM) symbiosis is a ubiquitous phenomenon, yet studies on its effect on aboveground natural enemies of herbivores are scarce and mainly deal with plant-mediated rather than herbivore-mediated interactions. Here, we studied herbivore-mediated effects of AM symbiosis on an acarine predator. We measured life history characteristics and population growth rates of Phytoseiulus persimilis preying on two-spotted spider mites, Tetranychus urticae, which were feeding on bean plants colonized or not colonized by the AM fungus Glomus mosseae. All major life history characteristics of P. persimilis, foremost oviposition rate, minimum prey requirements needed to reach adulthood, and developmental time, were positively affected by AM colonization of the host plant of their prey, together resulting in enhanced population growth rates of the predators. Hence, we hypothesize that a bottom-up trophic cascade may counteract the apparent negative effects of mycorrhizal symbiosis when promoting herbivory by promoting the predation of herbivores due to improved prey quality. We argue that this pathway may be involved in stabilizing plant-mycorrhizal symbiosis in ecosystems over time.

Plant-mediated aboveground-belowground interactions: the spider mite perspective

“…In fact, T. urticae feeding on mycorrhizal bean plants was a more favorable prey for P. persimilis than T. urticae feeding on nonmycorrhizal plants. Thus, the positive effects of AM on the spider mites cascaded up to the next trophic level via changing the nutritional quality of the prey (Hoffmann et al, 2011a). P. persimilis' preference for AM spider mite prey (Hoffmann et al, 2011b) and stronger attraction to volatiles of spider mite-infested mycorrhizal plants than those of non-mycorrhizal plants (Schausberger et al, 2012) is therefore adaptive for the predatory mites.…”

“…Studies on direct effects of AM symbiosis on host plants are numerous whereas research on indirect interactions between AM and aboveground bi-and tritrophic systems have just recently gained popularity. Hoffmann et al (2009Hoffmann et al ( , 2011a scrutinized aboveground-belowground interactions using a model system consisting of the AM fungus Glomus mosseae Nicol. and Gerd., common bean plants Phaseolus vulgaris L., the herbivorous spider mite T. urticae and its specialized natural enemy, the predatory mite Phytoseiulus persimilis Athias-Henriot, or subsystems thereof.…”

Disease ecology across soil boundaries: effects of below-ground fungi on above-ground host–parasite interactions

“…A rapid growing literature suggests that below-ground and above-ground biota can be intimately connected through the traits of plants [9,10]. Below-ground organisms, such as root symbiotic fungi and decomposers, can change plant quality and, therefore, have a profound impact on above-ground herbivore and predator performance [11][12][13][14][15], biodiversity [10] and ecosystem processes [16]. Additionally, food plants can change herbivore quality and immune function, and/or interfere directly with parasite infection or growth [5,17,18].…”

Microbial Root Mutualists Affect the Predators and Pathogens of Herbivores above Ground: Mechanisms, Magnitudes, and Missing Links

“…Therefore, by affecting plant nutritional status, root microbes belowground can indirectly affect predators and parasitoids aboveground. For example, in the presence of AMF, the predatory mite P. persimilis has a greater oviposition rate and shorter development time due to the higher quality of its prey, the two-spotted spider mite Tetranychus urricae ( Figure 1A) (Hoffmann et al, 2011c). Additionally, plant nutrient status often affects herbivore size, which in turn influences predator and parasitoid performance (Hunter, 2016).…”

“…Plant size and architectural complexity are key determinants of foraging efficiencies of parasitoids, with increases in size and complexity reducing per capita foraging efficiency (Cloyd and Sadof, 2000;Gingras and Boivin, 2002), while increasing the diversity of alternative prey (Lawton, 1983;Fowler, 1985). Consequently, when oxeye daisies (Leucanthemum vulgare) grow larger through association with AMF, rates of parasitism of the leaf miner Chromatomyia Higher quantity and quality of T. urticae directly translate into higher fitness and population growth rate of the predatory mite Phytoseiulus persimilis (Hoffmann et al, 2011c). Female P. persimilis preferentially select eggs of T. urticae that are reared on AMF-associated bean plants due to their higher quality (Hoffmann et al, 2011b); additionally, they can "smell" AMF-associated plants because AMF increase the production of β-ocimene and β-caryophyllene in T. urticae-infested plants (Schausberger et al, 2012).…”