Amplification of plant volatile defence against insect herbivory in a warming Arctic tundra

Abstract

Plant-emitted volatile organic compounds (VOCs) play fundamental roles in atmospheric chemistry and ecological processes by contributing to aerosol formation1 and mediating species interactions2. Rising temperatures and the associated shifts in vegetation composition have been shown to be the primary drivers of plant VOC emissions in Arctic ecosystems3. Although herbivorous insects also strongly alter plant VOC emissions2, no studies have addressed the impact of herbivory on plant VOC emissions in the Arctic. Here, we show that warming dramatically increases the amount and alters the blend of VOCs released in response to herbivory. We observed that a tundra ecosystem subjected to warming, by open-top chambers, for 8 or 18 years showed a 4-fold increase in leaf area eaten by insect herbivores. Herbivory by autumnal moth (Epirrita autumnata) larvae and herbivory-mimicking methyl jasmonate application on the widespread circumpolar dwarf birch (Betula nana) both substantially increased emissions of terpenoids. The long-term warming treatments and mimicked herbivory caused, on average, a 2- and 4-fold increase in monoterpene emissions, respectively. When combined, emissions increased 11-fold, revealing a strong synergy between warming and herbivory. The synergistic effect was even more pronounced for homoterpene emissions. These findings suggest that in the rapidly warming Arctic, insect herbivory may be a primary determinant of VOC emissions during periods of active herbivore feeding.

Natural Variation in Volatile Emissions of the Invasive Weed Calluna vulgaris in New Zealand

“…Elevated temperature is also known to increase the emission of various volatile compounds ranging from fatty acid derivatives to terpenoids [48][49][50], and these temperature-dependent emissions can be on both de novo synthesized and stored volatiles [51]. In this study, the emissions of (Z)-3hexenyl benzoate, germacrene D and (E)-DMNT by heather were affected by temperature differences between sites.…”

Insect Herbivory Strongly Modifies Mountain Birch Volatile Emissions

“…Both background herbivory and insect outbreaks are expected to increase with changing climate (Bale et al, 2002;Barrio et al, 2017) prompting further consequences on ecosystem functions. At high latitudes, insect herbivory may be the dominant factor increasing BVOC emissions during periods of active insect herbivore feeding (Li et al, 2019). Both temperature increases and higher insect herbivore pressure are likely crucial determinants of future BVOC emission rates in the high latitudes.…”

“…First, temperature has a strong, direct, positive effect on BVOC emission rates, as it increases BVOC synthesis and release in Arctic plants (Ghirardo et al, 2020). Second, increased insect herbivore activity acts to further increase BVOC emission rates and the two factors (temperature and herbivory) have synergistic effects (Li et al, 2019).…”

“…In the Arctic and Subarctic, few studies have analyzed BVOC emissions in response to insect herbivory (Mäntylä et al, 2008;Li et al, 2019). This is a paradox given the important role insect herbivores play as drivers of ecosystem functions in high-latitude environments (Jepsen et al, 2013;Lund et al, 2017;Vindstad et al, 2019).…”

“…One of the few recent studies that analyzed BVOC emissions following insect herbivory in the Subarctic found that herbivorymimicking methyl jasmonate (MeJa) application caused a fourfold increase in monoterpene emissions and a two-fold increase in sesquiterpene emissions from the dwarf birch, B. nana, compared to branches without MeJa application (Li et al, 2019). However, more field studies are required to quantify herbivory-BVOC emission relationships as we face potential distribution shifts in insect herbivores towards higher elevations/latitudes and increases in background herbivory, and insect outbreaks, with changing climate.…”