Herbivores and mycorrhizal fungi are important associates of most plants, but little is known about how these organisms interact. In a 9-yr experiment, we examined how the pinyon needle scale (Matsucoccus acalyptus) affects and is affected by the ectomycorrhizal mutualists found on the roots of scale-resistant and -susceptible pinyon pines (Pinus edulis). Three major results emerged. First, removal experiments demonstrated that scales negatively affected ectomycorrhiza. Second, although ectomycorrhiza could either positively or negatively influence scale performance by improving plant vigor or increasing plant investment in antiherbivore defenses, we found no ectomycorrhizal effect on scale mortality when we experimentally enhanced levels of ectomycorrhiza. This represented the first test of whether ectomycorrhiza promote plant resistance and contrasted with studies showing that arbuscular mycorrhiza negatively affected herbivores. Third, pinyon resistance to scales mediated the asymmetrical interaction between fungal mutualists and scale herbivores. High scale densities suppressed ectomycorrhizal colonization, but only on trees susceptible to scales. Similarities between mycorrhiza-herbivore interactions and competitive interactions among herbivores suggest broader generalities in the way aboveground herbivores interact with belowground plant associates. However, because mycorrhiza are mutualists, mycorrhiza-herbivore interactions do not fit within traditional competition paradigms. The widespread occurrence and importance of both herbivores and mycorrhiza argue for incorporating their interactions into ecological theory.
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