Early Root Herbivory Impairs Arbuscular Mycorrhizal Fungal Colonization and Shifts Defence Allocation in Establishing Plantago lanceolata

Abstract

Research into plant-mediated indirect interactions between arbuscular mycorrhizal (AM) fungi and insect herbivores has focussed on those between plant shoots and above-ground herbivores, despite the fact that only below-ground herbivores share the same part of the host plant as AM fungi. Using Plantago lanceolata L., we aimed to characterise how early root herbivory by the vine weevil (Otiorhynchus sulcatus F.) affected subsequent colonization by AM fungi (Glomus spp.) and determine how the two affected plant growth and defensive chemistry. We exposed four week old P. lanceolata to root herbivory and AM fungi using a 2×2 factorial design (and quantified subsequent effects on plant biomass and iridoid glycosides (IGs) concentrations. Otiorhynchus sulcatus reduced root growth by c. 64%, whereas plant growth was unaffected by AM fungi. Root herbivory reduced extent of AM fungal colonization (by c. 61%). O. sulcatus did not influence overall IG concentrations, but caused qualitative shifts in root and shoot IGs, specifically increasing the proportion of the more toxic catalpol. These changes may reflect defensive allocation in the plant against further attack. This study demonstrates that very early root herbivory during plant development can shape future patterns of AM fungal colonization and influence defensive allocation in the plant.

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

“…The reduction of AG herbivore growth should be attributed to other potentially induced defense traits, lower foliar nutrient values or physical defenses, which directly reduced leaf consumption by these herbivores. A shift in the relative composition of defense compounds can also lead to significant responses of herbivores (Bennett et al 2013), although it was not found in the current study (chapter 3). Another major finding in this thesis is that I observed that induced defense by AG herbivory in plant foliage against later conspecifics was canceled out when the plant roots were also exposed to feeding by BG herbivores (Figure 2.3).…”

“…Wireworms alone strongly reduced the levels of IGs in roots and increased the ratio of the more toxic compound catalpol relative to aucubin. The latter effect has been observed for other root herbivores as well (Bennett et al 2013). The reduction in root IG levels was initially counterbalanced by the increase in root IG levels caused by simultaneously introduced S. exigua.…”

“…However, the concentration of root IGs in P. lanceolata was not altered by AG herbivory in this study. Since the composition of IGs in P. lanceolata can also affect herbivore performance (Bennett et al 2013), I further measured the relative concentration of aucubin and catalpol, the main IGs in Plantago spp. I expected that AG herbivory shifted the composition of IGs, e.g.…”

“…Gange and West 1994, Fontana et al 2009, Schweiger et al 2014). Mycorrhization of P. lanceolata has been shown to suppress plant induced responses to aboveground herbivory and to alter the proportion of catalpol in the total IG level following herbivory Bennett et al 2013). …”

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

“…Because the commercial AMF mix that we used was purported to consist of four AMF species, the different effects of AMF availability on herbivore performance may be a function of differential colonization by AMF species under medium and high AMF availability. AMF species vary in their relative trading of nutrients (Lendenmann et al, 2011;Thonar et al, 2014;Argüello et al, 2016) and effects on plant phenotype (Gehring and Bennett, 2009;Bennett et al, 2013) which can alter herbivore performance (Roger et al, 2013;. However, cloning and sequencing of the AMF mix, and roots from milkweed plants grown under the same experimental conditions, with AMF-specific primers (Krüger et al, 2009) demonstrated that the AMF mix consisted only of F. mosseae (details in Supplementary Material).…”