Dataset Information

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 fourfold 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 two- and fourfold 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.

SUBMITTER: Li T

PROVIDER: S-EPMC6561779 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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

Li Tao T Holst Thomas T Michelsen Anders A Rinnan Riikka R

Nature plants 20190610 6

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 ...[more]

PMID: 31182843

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Project description:Current theory holds that the intensity of biotic interactions decreases with increases in latitude and elevation; however, empirical data demonstrate great variation in the direction, strength, and shape of elevational changes in herbivory. The latitudinal position of mountains may be one important source of this variation, but the acute shortage of data from polar mountains hampers exploration of latitude effects on elevational changes in herbivory. Here, we reduce this knowledge gap by exploring six elevation gradients located in three Arctic mountain ranges to test the prediction that a decrease in herbivory occurs with increasing elevation from forest to alpine tundra. Across the 10 most abundant evergreen and deciduous woody plant species, relative losses of foliage to insect herbivores were 2.2-fold greater at the highest elevations (alpine tundra) than in mid-elevation birch woodlands or low-elevation coniferous forests. Plant quality for herbivores (quantified by specific leaf area) significantly decreased with elevation across all studied species, indicating that bottom-up factors were unlikely to shape the observed pattern in herbivory. An experiment with open-top chambers established at different elevations showed that even a slight increase in ambient temperature enhances herbivory in Arctic mountains. Therefore, we suggest that the discovered increase in herbivory with elevation is explained by higher temperatures at the soil surface in open habitats above the tree line compared with forests at lower elevations. This explanation is supported by the significant difference in elevational changes in herbivory between low and tall plants: herbivory on low shrubs increased fourfold from forest to alpine sites, while herbivory on trees and tall shrubs did not change with elevation. We suggest that an increase in herbivory with an increase in elevation is typical for high-latitude mountains, where inverse temperature gradients, especially at the soil surface, are common. Verification of this hypothesis requires further studies of elevational patterns in herbivory at high latitudes.

Project description:Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature-dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13 CO2 -labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil-plant-atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13 C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%-44% (Salix) and 60%-68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%-58% (Salix) and 87%-95% (Betula). Analyses of above- and belowground 12/13 C showed shifts of C allocation in the plant-soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.

Dataset Information

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

Publications

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

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