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Title: Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between aboveground and belowground herbivores

item HUANG, WEI - Chinese Academy Of Sciences
item SIEMANN, E - Rice University
item YANG, X - Chinese Academy Of Sciences
item Wheeler, Gregory
item DING, J - Chinese Academy Of Sciences

Submitted to: Proceedings of the Royal Society B
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/21/2013
Publication Date: 7/31/2013
Publication URL:
Citation: Huang, W., Siemann, E., Yang, X., Wheeler, G.S., Ding, J. 2013. Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between aboveground and belowground herbivores. Proceedings of the Royal Society B. 280:1767. 2013.

Interpretive Summary: Insect feeding invokes a cascade of chemical changes in the damaged plant. Some of these changes involve primary nutrients such as nitrogen and carbohydrates, while other changes include secondary plant compounds such as tannins and flavonoids that can be involved in anti-herbivore defense. Chinese tallow (Triadica sebifera), an invasive plant in the southeastern U.S., disrupts ecosystems by competing with commercial forests and natural areas. Our research focuses on an insect being developed to control this weed, the flea beetle, Bikasha collaris which feeds as a larva on the tree roots while the adult beetle feeds on leaves above ground. In response to belowground larval damage, the roots had higher tannin concentrations but aboveground feeding by adults prevented this increase. Thus adult feeding doubled survival of belowground larvae. Aboveground feeding by adults elevated root nitrogen which contributed to the increased larval survival. Aboveground feeding also increased the tannin levels in the foliage and this increase was amplified with larval root damage resulting in decreased adult survival. As tannins increased in either the roots or stems, the levels of flavonoids decreased. These results highlight the reciprocal nature of this plant’s responses to aboveground and belowground damage. Moreover, they suggest that the insects feeding on these plants may benefit from these plant responses.

Technical Abstract: To date, it remains unclear how herbivore-induced changes in plant primary and secondary metabolites impact aboveground and belowground herbivore interactions. Here we report the effects of aboveground (adult) and belowground (larval) feeding by Bikasha collaris on nitrogen and secondary chemicals in shoots and roots of Triadica sebifera to explain reciprocal aboveground and belowground insect interactions. Plants increased root tannins with belowground herbivory but aboveground herbivory prevented this increase, doubling larval survival. Aboveground herbivory elevated root nitrogen, likely contributing to increased larval survival. However, plants increased foliar tannins with aboveground herbivory and belowground herbivory amplified this increase, decreasing adult survival. As either foliar or root tannins increased, foliar flavonoids decreased, suggesting a tradeoff between these chemicals. Together these results show that plant chemicals mediate the contrasting effects of conspecific larval and adult insects while insects may take advantage of plant responses to facilitate their offspring performance which may influence population dynamics.