Three-Way Interactions among Mutualistic Mycorrhizal Fungi, Plants, and Plant Enemies: Hypotheses and Synthesis

Abstract

A number of studies have shown that an association with mycorrhizal fungi can alter the outcome of interactions between plants and their enemies. While the directions of these effects vary, their strength suggests the need for greater attention to multispecies interactions among plant enemies, plants, and mycorrhizal fungi. We recognize that mycorrhizal fungi could effect plant enemies by improving plant nutrition, modifying plant tolerance, or modifying plant defenses. In addition, mycorrhizal fungi could directly interfere with pathogen infection, herbivory, or parasitism by occupying root space. We formalize these alternative outcomes of multispecies interactions and explore the long-term dynamics of the plant-enemy interactions based on these different scenarios using a general model of interactions between plants and plant enemies. We then review the literature in terms of the assumptions of the alternative mechanisms and the predictions of these models. Through this effort, we identify new directions in the study of tritrophic interactions between enemies, plants, and soil mutualists.

Tomato leafminer [(Tuta absoluta Meyrick) (Lepidoptera: Gelechiidae)] and its current ecofriendly management strategies: A review

“…Systemic responses that plant root microorganisms cause emission of volatiles at aerial parts of plants in multitrophic interactions that attract above-ground parasitoids (Bruce and Pickett, 2007). Furthermore, plants interacting with beneficial microbes can also benefit from an increase in tolerance to herbivory (Bennett et al, 2008;Vannette and Hunter, 2008). This can be achieved by improving nutrient and water uptake facility for better plant development.…”

Interactions of ectomycorrhizas and above-ground insect herbivores on silver birch

“…1,2 Negative impact of mycorrhizas may come via altered carbon/nitrogen (C/N) ratio of host plants, i.e., mycorrhizal plants invest more C for antiherbivore defense which might decrease herbivore performance. 1,[3][4][5] Interestingly, all plants have not evolved equal level of defense and generalist insects are deterred by high concentrations of defense compounds, whereas specialists use them to identify their suitable host plants. 6 Also the fact that insects with various feeding guilds respond differently to the host plant stress 7 is bringing more complexity to mycorrhiza-insect herbivore interaction studies.…”

Arriving at the right time : a temporal perspective on above-belowground herbivore interactions

“…They can either positively influence aboveground herbivores through improving plant vigor and foliar nutrient concentrations (Borowicz 1997) but also negatively affect foliar herbivores through changes in constitutive and inducible defenses against herbivory (Bennett et al 2006). Indeed mycorrhizal colonization can significantly increase the concentration of defense compounds, including iridoid glycosides (Gange and West 1994) and alkaloids (AbuZeyad et al 1999) that can strongly reduce performance and growth of some aboveground herbivores.…”

“…AMF can interact with aboveground herbivores via multiple mechanisms (Bennett et al 2006;Gehring and Bennett 2009). They can either positively influence aboveground herbivores through improving plant vigor and foliar nutrient concentrations (Borowicz 1997) but also negatively affect foliar herbivores through changes in constitutive and inducible defenses against herbivory (Bennett et al 2006).…”

“…This subsequently can alter the plant responses to its herbivores. These mycorrhizae-induced changes in the plant can be either beneficial or detrimental for herbivores that feed on the plant, and the strength and direction of these effects may depend on the feeding mode or specialization of the herbivore (Bennett et al 2006;Koricheva et al 2009;Borowicz 2013). A meta-analysis of 34 studies showed that arbuscular mycorrhizal fungi (AMF) predominantly have negative effects on the performance of generalist chewing herbivores, but that they can enhance the performance of specialist chewing herbivores (Koricheva et al 2009).…”