Abstract
Aboveground plant performance is strongly influenced by belowground microorganisms, some of which are pathogenic and have negative effects, while others, such as nitrogen-fixing bacteria and arbuscular mycorrhizal fungi, usually have positive effects. Recent research revealed that belowground interactions between plants and functionally distinct groups of microorganisms cascade up to aboveground plant associates such as herbivores and their natural enemies. However, while functionally distinct belowground microorganisms commonly co-occur in the rhizosphere, their combined effects, and relative contributions, respectively, on performance of aboveground plant-associated organisms are virtually unexplored. Here, we scrutinized and disentangled the effects of free-living nitrogen-fixing (diazotrophic) bacteria Azotobacter chroococcum (DB) and arbuscular mycorrhizal fungi Glomus mosseae (AMF) on host plant choice and reproduction of the herbivorous two-spotted spider mite Tetranychus urticae on common bean plants Phaseolus vulgaris. Additionally, we assessed plant growth, and AMF and DB occurrence and density as affected by each other. Both AMF alone and DB alone increased spider mite reproduction to similar levels, as compared to the control, and exerted additive effects under co-occurrence. These effects were similarly apparent in host plant choice, that is, the mites preferred leaves from plants with both AMF and DB to plants with AMF or DB to plants grown without AMF and DB. DB, which also act as AMF helper bacteria, enhanced root colonization by AMF, whereas AMF did not affect DB abundance. AMF but not DB increased growth of reproductive plant tissue and seed production, respectively. Both AMF and DB increased the biomass of vegetative aboveground plant tissue. Our study breaks new ground in multitrophic belowground–aboveground research by providing first insights into the fitness implications of plant-mediated interactions between interrelated belowground fungi–bacteria and aboveground herbivores.
Highlights
Plants are the prime links between the below- and aboveground spheres, mediating interactions between belowand aboveground living organisms that do not directly interact with each other
The effects of single belowground microorganism species on aboveground plant-associated herbivores are relatively well understood, but virtually nothing is known about the combined effects of functionally distinct belowground microorganisms on the interactions between aboveground plant parts, herbivores, and carnivores
We scrutinized the interrelated effects of two primarily plant-mutualistic belowground microorganisms, a mycorrhizal fungus and a free-living nitrogen-fixing bacterium, on herbivores feeding on aboveground plant parts
Summary
Plants are the prime links between the below- and aboveground spheres, mediating interactions between belowand aboveground living organisms that do not directly interact with each other. Based on intensive research during the past two decades, it is generally acknowledged that below- and aboveground plant-associated processes are mutually dependent (Van der Putten et al 2001; Bezemer and van Dam 2005; Rasmann and Turlings 2007; Erb et al 2008; Koricheva et al 2009; Heil 2011; van Dam and Heil 2011; Schausberger et al 2012). Aboveground plant performance is strongly influenced by belowground microorganisms, which may be either pathogens or mutualists, which in turn affects herbivorous organisms inhabiting and feeding a 2015 The Authors. Concurrent associations with AMF and nitrogen fixers (RB or DB) commonly act additively or synergistically on nutrient uptake by the plants Under certain circumstances, competition for nutrients, space, or other resources between AMF and nitrogen fixers may occur, resulting in subtractive effects as compared to the predicted sum of each symbiont’s effect (Scheublin and van der Heijden 2006)
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