, Volume 184, Issue 2, pp 497–506 | Cite as

Colonization by nitrogen-fixing Frankia bacteria causes short-term increases in herbivore susceptibility in red alder (Alnus rubra) seedlings

  • Daniel J. Ballhorn
  • Jacob D. Elias
  • M. A. Balkan
  • Rachel F. Fordyce
  • Peter G. Kennedy
Plant-microbe-animal interactions - original research


Carbon allocation demands from root-nodulating nitrogen-fixing bacteria (NFB) can modulate the host plant’s chemical phenotype, with strong bottom–up effects on herbivores. In contrast to well-studied rhizobia, the effects of other important NFB on plant chemistry and herbivory are much less understood. Here, combining field surveys in the Oregon Coast Range, USA with laboratory experiments, we analyzed how N2-fixing Frankia bacteria influenced plant growth, chemistry, and herbivory on Alnus rubra (red alder) seedlings. In the field, we quantified Frankia nodulation, herbivore damage, and plant size. In the laboratory, we grew seedlings with Frankia (F+), Frankia-free but nitrogen-fertilized (N+), or both uncolonized and unfertilized (F−N−) and assessed growth and leaf chemistry. We further conducted choice trials with black slugs, Arion rufus, a natural red alder herbivore. In the field, Frankia nodulation was significantly positively correlated with herbivory and negatively with seedling height. In contrast, in the lab, F+ as well as N+ seedlings were significantly taller than the F−N− controls. Seedlings from both treatments also had significantly increased leaf protein concentration compared to controls, whereas carbon-based nutritive compounds (carbohydrates) as well as leaf palatability-decreasing condensed tannins, lignin, and fiber were decreased in F+ but not in N+ treatments. In the choice assays, slugs preferred leaf material from F+ seedlings, but the effects were only significant in young leaves. Our study indicates that colonization by Frankia causes short-term ecological costs in terms of susceptibility to herbivory. However, the ubiquity of this symbiosis in natural settings suggests that these costs are outweighed by benefits beyond the seedling stage.


Trophic interactions Ecological costs Nitrogen fixation Condensed tannins Pacific Northwest Plant defense Plant–herbivore interactions 



The authors thank V. Engebretson for assistance with experimental setup and maintenance. Funding was provided by the National Science Foundation (IOS # 1457369 and IOS # 1656057 to DJB and DEB # 1020735 to PGK).

Author contribution statement

DJB and PGK conceived and designed the experiments. DJB, PGK, and RFF performed the experiments. DJB, PGK, and JDE analyzed the data. DJB, PGK, JDE, and MAB co-wrote the manuscript.


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Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Daniel J. Ballhorn
    • 1
  • Jacob D. Elias
    • 1
    • 2
  • M. A. Balkan
    • 1
  • Rachel F. Fordyce
    • 1
    • 3
  • Peter G. Kennedy
    • 4
  1. 1.Department of BiologyPortland State UniversityPortlandUSA
  2. 2.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  3. 3.Department of Plant BiologyUniversity of CaliforniaDavisUSA
  4. 4.Department of Plant BiologyUniversity of MinnesotaSt. PaulUSA

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