The volatile emission of a specialist herbivore alters patterns of plant defence, growth and flower production in a field population of goldenrod

Abstract

Summary Plants frequently employ induced, rather than constitutive, defences against herbivores and pathogens, presumably as an adaptive response to the unpredictability of attack by particular antagonists. Plants may further accelerate defence deployment by ‘priming’ appropriate defences in response to environmental cues that reliably predict impending attack. However, the population‐ and community‐level ecological consequences of such priming remain relatively unexplored. We recently discovered that the volatile emissions of male Eurosta solidaginis prime the antiherbivore defences of its host plant, tall goldenrod (Solidago altissima). This co‐evolved system provides a unique opportunity to study the ecological consequences of priming in a natural system. We explored effects of the priming cue on neighbouring ramets at varying distances from the emission source by quantifying subsequent levels of foliar herbivory, as well as plant growth and flower production (which might reveal trade‐offs between investment in growth or reproduction and defence). We observed a linear increase in leaf damage with distance from the emission source (up to our maximal distance of 1 m), consistent with the hypothesis that the intensity of priming corresponds to the intensity of exposure to the fly emission. Unexpectedly, ramets nearest the emission source also exhibited a short‐term increase in growth‐rate; however, this effect did not persist to the end of the season or increase flower production. Instead, ramet's mid‐distance from the emission source exhibited reduced growth and flower production compared to those nearer or farther away. Synthesis. The responsiveness of Solidago altissima ramets to herbivore‐associated cues across a distance of 1 m or more is highly relevant in this system, where individual ramets frequently grow within a few cm of one another. Furthermore, the resulting mosaic of ramets primed to varying degrees might influence herbivore (and consequently predator) distributions. The unexpected decline in flower production by mid‐distance ramets suggests that the effects of plant priming on ecological interactions among plants and other organisms (such as tritrophic interactions and competition) may feed back onto plant fitness in complex, and as yet unexplored, ways. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12826/suppinfo is available for this article.

Identification of an insect-produced olfactory cue that primes plant defenses

“…Our results indicate that S. altissima plants respond to exposure to smaller amounts of E,S -conophthorin than typically emitted by males (1% of two MDE). These findings complement the results of field studies indicating that priming of defenses in neighboring plants by the Eurosta emission can occur over distances of at least 1 m within dense stands of S. altissima 47 . Thus, given the observed sensitivity of S. altissima to E,S -conophthorin, neighboring plants—which will often be ramets of the same genet as the stem on which an emitting male is perched—are also likely to exhibit priming responses.…”

“…This may have ecological significance, as these adjacent stems are also likely targets for oviposition by female flies 42 . Furthermore, such responses could have important implications for the spatial distribution of E. solidaginis galls and other herbivorous species on S. altissima within a population of plants, as well as for plant-plant interactions among S. altissima individuals 47 .…”

Chemical cues linked to risk: Cues from below‐ground natural enemies enhance plant defences and influence herbivore behaviour and performance

“…This could be a “better safe than sorry” approach, where plants are highly sensitive to environmental cues they associate with risk and respond by priming their defences (Orrock et al, ). As an alternative to inducing defences, priming arguably incurs little to no fitness cost for plants even in the absence of actual herbivore attack (Martinez‐Medina et al, ; Yip, De Moraes, Mescher, & Tooker, ). An intriguing finding in this study was the subtle difference in plant responses to EPNs or their associated chemical cues.…”

Plant volatiles induced by herbivore eggs prime defences and mediate shifts in the reproductive strategy of receiving plants

“…For example, sagebrush exposed to cues from damaged neighbours increased the production of inflorescences and lateral branches at the expense of vertical growth (Karban et al 2012; Karban 2017), while tobacco plants exposed to damaged (manually clipped)‐sagebrush neighbours produced more flowers and seeds than plants with undamaged neighbours (Karban & Maron 2002). Exposure to the putative sex pheromone of a gall‐inducing fly was also shown to increase short‐term growth in goldenrod plants (Yip et al 2017).…”