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

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)497-506
Number of pages10
JournalOecologia
Volume184
Issue number2
DOIs
StatePublished - Jun 1 2017

Fingerprint

Alnus rubra
Frankia
herbivore
herbivores
colonization
seedling
bacterium
seedlings
nitrogen
bacteria
herbivory
nitrogen-fixing bacteria
slugs
nodulation
slug
leaves
chemistry
phytochemistry
Arion
palatability

Keywords

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

Cite this

Colonization by nitrogen-fixing Frankia bacteria causes short-term increases in herbivore susceptibility in red alder (Alnus rubra) seedlings. / Ballhorn, Daniel J.; Elias, Jacob D.; Balkan, M. A.; Fordyce, Rachel F.; Kennedy, Peter G.

In: Oecologia, Vol. 184, No. 2, 01.06.2017, p. 497-506.

Research output: Contribution to journalArticle

Ballhorn, Daniel J. ; Elias, Jacob D. ; Balkan, M. A. ; Fordyce, Rachel F. ; Kennedy, Peter G. / Colonization by nitrogen-fixing Frankia bacteria causes short-term increases in herbivore susceptibility in red alder (Alnus rubra) seedlings. In: Oecologia. 2017 ; Vol. 184, No. 2. pp. 497-506.
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