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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.

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Fig. 1: Individual and joint impacts of in situ warming and mimicked herbivory on VOC emissions.
Fig. 2: Impacts of warming and mimicked herbivory on VOC blends.
Fig. 3: Time course of VOC induction.
Fig. 4: Impacts of in situ warming on background insect herbivory.

Data availability

All VOC and background herbivory data that support the findings of this study are available in Figshare with the data DOI identifier https://doi.org/10.6084/m9.figshare.7879340.

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Acknowledgements

We thank M. Jylkkä for providing the image of E. autumnata and C.L. Davie-Martin for language editing. We gratefully acknowledge financial support from the Danish Council for Independent Research/Natural Sciences, the Danish National Research Foundation (grant No. CENPERM DNRF100), the Marie Sklodowska-Curie grant (No. 751684) and the European Research Council (grant No. 771012) under the European Union’s Horizon 2020 research and innovation programme. The Abisko Scientific Research Station (Sweden) is thanked for housing and logistics support.

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Authors and Affiliations

Authors

Contributions

T.L. and R.R. designed the experiment. A.M. established the experimental site. T.L. and T.H. developed the methodology for the volatile emission time course experiments. T.L. collected, analysed and interpreted the data and wrote the manuscript. All authors commented on the manuscript and approved the final version.

Corresponding author

Correspondence to Tao Li.

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The authors declare no competing interests.

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Journal Peer Review Information: Nature Plants thanks Robert Hollister and the other anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary information

Supplementary Figs. 1–10.

Reporting Summary.

Supplementary Tables 1–6

Supplementary Table 1: VOC emissions of Betula nana under different treatments. Supplementary Table 2: Summary of mixed-effects models testing for main warming and mimicked herbivory effects and their interactions. Supplementary Table 3: Summary of Kruskal–Wallis tests for warming and herbivory effects. Supplementary Table 4: Timelines of real time measurements of VOC emissions. Supplementary Table 5: List of ion masses and molecular formulae measured with the PTR–ToF–MS. Supplementary Table 6: Summary of mixed-effects models testing for warming, litter addition, herbivory effects and their interactions.

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Li, T., Holst, T., Michelsen, A. et al. Amplification of plant volatile defence against insect herbivory in a warming Arctic tundra. Nat. Plants 5, 568–574 (2019). https://doi.org/10.1038/s41477-019-0439-3

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