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.
Highlights
It is accepted that terrestrial plants mediate interactions between organisms associated with them, often shaping ecosystem processes and community structure [1,2]
Otiorhynchus sulcatus larvae used in this experiment were offspring of adults collected at night from plants and bushes surrounding the aforementioned P. lanceolata population
The repeated measures analysis of variance (ANOVA) revealed that P. lanceolata growth was significantly affected by time (F4,140 = 9.32, p,0.0001, Figure 2, Table 2), the interaction of time and block (F4,140 = 5.31, p = 0.0005, Table 2), and the interaction of time and vine weevil (F4,140 = 8.97, p,0.0001, Table 2), but that the effect of arbsucular mycorrhizal (AM) fungal inoculation did not vary with time
Summary
It is accepted that terrestrial plants mediate interactions between organisms associated with them, often shaping ecosystem processes and community structure [1,2]. Interactions between herbivorous insects and plant-associated fungi have become especially well studied, with numerous examples involving plant pathogens [3,4], endophytes [5,6] and symbionts Plant-mediated effects of arbsucular mycorrhizal (AM) fungi have been shown to be beneficial, detrimental or neutral for herbivore fitness (reviewed in [9,10]), and the evolutionary outcomes have been explored [7]. It has been suggested that AM fungal-induced increases in defensive chemical concentrations lead to an increased selective advantage for plants in plant-herbivore interactions [7]. Given that root herbivores and AM fungi exploit the same part of the plant, either simultaneously or at different times, it seems likely that root herbivory influences AM fungal colonization. AM fungi can negatively (e.g. [13,14]) or positively (e.g. [15]) affect root herbivores, whereas chewing root herbivores may stimulate [15,16], or have no effect on (e.g. [13,14]) AM fungal colonization
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