From Plants to Birds: Higher Avian Predation Rates in Trees Responding to Insect Herbivory

BACKGROUND: An understanding of the evolution of potential signals from plants to the predators of their herbivores may provide exciting examples of co-evolution among multiple trophic levels. Understanding the mechanism behind the attraction of predators to plants is crucial to conclusions about co-evolution. For example, insectivorous birds are attracted to herbivore-damaged trees without seeing the herbivores or the defoliated parts, but it is not known whether birds use cues from herbivore-damaged plants with a specific adaptation of plants for this purpose. METHODOLOGY: We examined whether signals from damaged trees attract avian predators in the wild and whether birds could use volatile organic compound (VOC) emissions or net photosynthesis of leaves as cues to detect herbivore-rich trees. We conducted a field experiment with mountain birches (Betula pubescens ssp. czerepanovii), their main herbivore (Epirrita autumnata) and insectivorous birds. Half of the trees had herbivore larvae defoliating trees hidden inside branch bags and half had empty bags as controls. We measured predation rate of birds towards artificial larvae on tree branches, and VOC emissions and net photosynthesis of leaves. PRINCIPAL FINDINGS AND SIGNIFICANCE: The predation rate was higher in the herbivore trees than in the control trees. This confirms that birds use cues from trees to locate insect-rich trees in the wild. The herbivore trees had decreased photosynthesis and elevated emissions of many VOCs, which suggests that birds could use either one, or both, as cues. There was, however, large variation in how the VOC emission correlated with predation rate. Emissions of (E)-DMNT [(E)-4,8-dimethyl-1,3,7-nonatriene], beta-ocimene and linalool were positively correlated with predation rate, while those of highly inducible green leaf volatiles were not. These three VOCs are also involved in the attraction of insect parasitoids and predatory mites to herbivore-damaged plants, which suggests that plants may not have specific adaptations to signal only to birds

The volatile organic compound (VOC) emissions from herbivore (black bars) and control (grey bars) birch branches (ls means+SE from statistical models are shown).

<p>A) six days, <i>n</i> = 14 in both control and herbivore trees, and B) 10–11 days since the start of defoliation by autumnal moth larvae, control: <i>n</i> = 7 and herbivore: <i>n</i> = 6. Compounds: (1) α-pinene, (2) β-myrcene, (3) limonene, (4) β-ocimene, (5) linalool, (6) (<i>E</i>)-DMNT, (7) α-copaene, (8) α-humulene, (9) caryophyllene oxide, (10) (<i>E</i>)-β-caryophyllene, (11) β-bourbonene, (12) cis-3-hexenyl acetate, (13) cis-3-hexen-1-ol+(<i>E</i>)-2-hexenal, (14) nonanal, (15) cis-3-hexenyl butyrate. (*: <i>p</i><0.05; **: <i>p</i><0.01; ***: <i>p</i><0.001).</p

Photos of the real and the artificial larvae.

<p>A) A fifth instar <i>Epirrita autumnata</i> larva on a branch. B) Larval feeding damage on mountain birch (<i>Betula pubescens</i> ssp. <i>czerepanovii</i>) leaves. C) A plasticine larva on a mountain birch branch. D). A beak marking on a plasticine larva indicating a predation attempt by an insectivorous bird.</p

Spearman's rank correlation coefficients (<i>r</i>_S) between individual volatile organic compound emissions in the first measurement (6 days after the start of defoliation) and the total sum of damaged plasticine larvae per tree (<i>n</i> = 28 trees) in both herbivore and control trees.

<p>Column ‘No.’ refers to the number of the compound in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002832#pone-0002832-g002" target="_blank">Figure 2</a>. Column ‘Group’ indicates into which group of VOCs the compound belongs. (^*: <i>p</i><0.05; ^**: <i>p</i><0.01).</p

The daily numbers of damaged plasticine larvae found from herbivore (black bars) and control (grey bars) birches.

<p>The X-axis shows the number of days since the start of defoliation by autumnal moth larvae in the herbivore trees. Solid and hatched arrows show the days when the volatile organic compounds (VOCs) and net photosynthesis rate, respectively, were measured.</p

Scatter plots of three volatile organic compounds (VOCs) and the total sum of damaged plasticine larvae in herbivore (black dots) and control (grey dots) trees (<i>n</i> = 28). A) (<i>E</i>)-DMNT, B) linalool and C) β-ocimene.

<p>Note the different x-axes in the panels.</p