Letter

Insect herbivory alters impact of atmospheric change on northern temperate forests

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Published online:

Abstract

Stimulation of forest productivity by elevated concentrations of CO2 is expected to partially offset continued increases in anthropogenic CO2 emissions. However, multiple factors can impair the capacity of forests to act as carbon sinks; prominent among these are tropospheric O3 and nutrient limitations1,2. Herbivorous insects also influence carbon and nutrient dynamics in forest ecosystems, yet are often ignored in ecosystem models of forest productivity. Here we assess the effects of elevated levels of CO2 and O3 on insect-mediated canopy damage and organic matter deposition in aspen and birch stands at the Aspen FACE facility in northern Wisconsin, United States. Canopy damage was markedly higher in the elevated CO2 stands, as was the deposition of organic substrates and nitrogen. The opposite trends were apparent in the elevated O3 stands. Using a light-use efficiency model, we show that the negative impacts of herbivorous insects on net primary production more than doubled under elevated concentrations of CO2, but decreased under elevated concentrations of O3. We conclude that herbivorous insects may limit the capacity of forests to function as sinks for anthropogenic carbon emissions in a high CO2 world.

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References

  1. 1.

    et al. Free-Air exposure systems to scale up ozone research to mature trees. Plant Biol. 9, 181–190 (2007).

  2. 2.

    et al. Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440, 922–925 (2010).

  3. 3.

    Forests and climate change: forcings, feedbacks, and the climate benefit of forests. Science 320, 1444–1449 (2008).

  4. 4.

    , Ecological lessons from Free-Air CO2 Enrichment (FACE) experiments. Annu. Rev. Ecol. Evol. Syst. 42, 181–203 (2011).

  5. 5.

    et al. Tropospheric ozone moderates responses of temperate hardwood forests to elevated CO2: a synthesis of molecular to ecosystem results from the Aspen FACE project. Funct. Ecol. 17, 289–304 (2003).

  6. 6.

    , What have we learned from 15 years of free-air CO2 (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant productivity to rising CO2. New Phytol. 165, 351–372 (2005).

  7. 7.

    , , , , Quantifying the impact of future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta-analysis. Global Change Biol. 15, 396–424 (2009).

  8. 8.

    , , , Rising concentrations of atmospheric CO2 have increased growth in natural stands of quaking aspen (Populus tremeuloides). Global Change Biol. 16, 2186–2197 (2010).

  9. 9.

    , Stand structure and development after gypsy moth defoliation in the Appalachian Plateau. Forest Ecol. Manag. 89, 79–88 (1998).

  10. 10.

    et al. Insect defoliation and nutrient cycling in forests. BioScience 52, 335–341 (2002).

  11. 11.

    et al. Using light-use and production efficiency models to predict photosynthesis and net carbon exchange during forest canopy disturbance. Ecosystems 11, 26–44 (2008).

  12. 12.

    , , , Herbivore-mediated material fluxes in a northern deciduous forest under elevated carbon dioxide and ozone concentrations. New Phytol. 204, 397–407 (2014).

  13. 13.

    , , Atmospheric change alters foliar quality of host trees and performance of two outbreak insect species. Oecologia 168, 863–876 (2012).

  14. 14.

    , Atmospheric change alters performance of an invasive forest insect. Global Change Biol. 18, 3543–3557 (2012).

  15. 15.

    , , Elevated carbon dioxide and ozone have weak, idiosyncratic effects on herbivorous forest insect abundance, species richness, and community composition. Insect Conserv. Diver. 7, 553–562 (2014).

  16. 16.

    , Elevated atmospheric carbon dioxide and ozone alter forest insect abundance and community composition. Insect Conserv. Diver. 1, 233–241 (2008).

  17. 17.

    Impacts of atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J. Chem. Ecol. 36, 2–21 (2010).

  18. 18.

    et al. Insect herbivory in an intact understory experimental CO2 enrichment. Oecologia 138, 566–573 (2004).

  19. 19.

    et al. Effects if elevated CO2 and O3 on leaf damage and insect abundance in a soybean agroecosystem. Arthropod Plant Interact. 2, 125–135.

  20. 20.

    , , , , CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc. Natl Acad. Sci. USA 107, 19368–19373 (2010).

  21. 21.

    et al. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience 54, 731–739 (2004).

  22. 22.

    et al. Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol. Lett. 14, 349–357 (2011).

  23. 23.

    , , , Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol. Lett. 14, 1220–1226 (2011).

  24. 24.

    , , Enhanced root exudation indices microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol. Lett. 14, 187–194 (2012).

  25. 25.

    et al. Global response of terrestrial ecosystem structure and function to CO2 and climate change: results from six dynamic global vegetation models. Global Change Biol. 7, 357–373 (2001).

  26. 26.

    et al. Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using five Dynamic Global Vegetation Models (DGVMs). Global Change Biol. 14, 2015–2039 (2008).

  27. 27.

    , , Little strokes fell great oaks: minor but chronic herbivory substantially reduces birch growth. Oikos 121, 2036–2043 (2012).

  28. 28.

    et al. Elevated carbon dioxide and ozone alter productivity and ecosystem carbon content in northern temperate forests. Global Change Biol. 20, 2492–2504 (2014).

  29. 29.

    , , Foliar morphology and canopy nitrogen as predictors of light-use efficiency in terrestrial vegetation. Agr. Forest Meterol. 115, 163–171 (2003).

  30. 30.

    , , Direct and indirect estimation of leaf area index, fAPAR, and net primary production of terrestrial ecosystems. Remote Sens. Environ. 70, 29–51 (1999).

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Author information

Author notes

    • J. J. Couture

    Present address: Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA.

Affiliations

  1. Department of Entomology, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA

    • J. J. Couture
    • , T. D. Meehan
    •  & R. L. Lindroth
  2. Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA

    • E. L. Kruger

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Contributions

R.L.L. designed the experiment and secured funding for the project; J.J.C. and T.D.M. collected field and laboratory data; J.J.C. and E.L.K. designed and performed the modelling exercise relating canopy damage to forest productivity; J.J.C. analysed the data and wrote the manuscript with the participation of R.L.L., T.D.M. and E.L.K.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to J. J. Couture.

Supplementary information