Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores

Abstract

Plants attacked by insects may induce defenses locally in attacked plant tissues and/or systemically in non-attacked tissues, such as aboveground herbivory affecting belowground roots or belowground herbivory modifying aboveground tissues (i.e., cross-compartment systemic defense). Through induced systemic plant defenses, above-and belowground insect herbivores indirectly interact when feeding on a shared host plant. However, determining the systemic effects of herbivory on cross-compartment plant tissues and cascading consequences for herbivore communities remains underexplored. The goal of this study was to determine how belowground striped cucumber beetle (Acalymma vittatum) larval herbivory alters aboveground zucchini squash (Cucurbita pepo subsp. pepo) defenses and interactions with herbivores, including adult cucumber beetles and squash bugs (Anasa tristis). To explore this question, field and laboratory experiments were conducted to compare responses of aboveground herbivores to belowground larvae-damaged plants and non-damaged control plants. We also characterized changes in defensive chemicals and nutritional content of aboveground plant structures following belowground herbivory. We discovered belowground herbivory enhanced aboveground plant resistance and deterred aboveground foraging herbivores. We also found that larvae-damaged plants emitted higher amounts of a key volatile compound, (E)-β-ocimene, compared to non-damaged controls. Further investigation suggests that other mechanisms, such as plant nutrient content, may additionally contribute to aboveground herbivore foraging decisions. Collectively, our findings underscore connections between above-and belowground herbivore communities as mediated through induced systemic defenses of a shared host plant. Specifically, these findings indicate that belowground larval herbivory systemically enhances plant defenses and deters a suite of aboveground herbivores, suggesting larvae may manipulate aboveground plant defenses for their own benefit, while plants may benefit from enhanced systemic defenses against multi-herbivore attack.

Belowground insect herbivory induces systemic volatile emissions that strengthen neighbouring plant resistance aboveground

“…In this study, we characterised systemic aboveground volatiles of nondamaged and belowground larvae‐damaged plants. We found an increase in aboveground emission of ( E )‐β‐ocimene from belowground larvae‐damaged plants, which mirrored previous findings in a different squash cultivar (Thompson et al, 2022). Similarities in systemic HIPVs across cultivars suggest ( E )‐β‐ocimene may be a conserved signal of herbivory in squash, providing new insights into systemic defence induction and plant signalling in this system.…”

“…In response to herbivory, plants can redistribute nutrients and shift resources away from insects (Johnson et al, 2009; Orians et al, 2011; Steinbrenner et al, 2011), indicating HIPV‐exposure could possibly preempt nutrient changes that reduce squash bug performance. Notably, our previous research detected similar changes in plant nutrients: belowground larval herbivory increased aboveground protein content and the ratio of protein: carbohydrates, while decreasing aboveground carbohydrates (Thompson et al, 2022). We further demonstrated that squash bugs avoided larvae‐damaged plants, preferring to settle and lay eggs on nondamaged control plants (Thompson et al, 2022).…”

“…During the third collection period (6:00–14:00) in the light, we detected an increase in systemic aboveground emission of ( E )‐β‐ocimene from larvae‐damaged plants relative to controls (Figure 3; ANOVA, F = 5.77, p = 0.03). Given the ecological relevance of ( E )‐β‐ocimene from previous work in this system (Thompson et al, 2022), we quantified changes in aboveground emission of ( E )‐β‐ocimene across the 24 h collection period. Larvae‐damaged plants emitted higher amounts of ( E )‐β‐ocimene over the total 24 h collection period (Supporting Information S1: Figure ; ANOVA, F = 5.24, p = 0.03).…”

“…Striped cucumber beetles and squash bugs represent unique but often simultaneous threats to squash, and plants likely face bouts of multi‐herbivore attack aboveground and belowground (Barber et al, 2015; Brzozowski et al, 2021). Further, our previous research found that belowground striped cucumber beetle larvae induce systemic changes in aboveground squash tissues, including triggering systemic HIPVs and enhancing emission of the compound ( E )‐β‐ocimene (Thompson et al, 2022). We also discovered that adult striped cucumber beetles and squash bugs avoid larvae‐damaged plants, preferring to settle and feed on nondamaged plants (Thompson et al, 2022).…”

“…Further, our previous research found that belowground striped cucumber beetle larvae induce systemic changes in aboveground squash tissues, including triggering systemic HIPVs and enhancing emission of the compound ( E )‐β‐ocimene (Thompson et al, 2022). We also discovered that adult striped cucumber beetles and squash bugs avoid larvae‐damaged plants, preferring to settle and feed on nondamaged plants (Thompson et al, 2022). Building on these findings, the current research investigates if squash plants can detect and respond to systemic HIPVs from their larvae‐damaged neighbours and strengthen their defences accordingly.…”