, Volume 175, Issue 1, pp 187–198 | Cite as

Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

  • Minggang Wang
  • Arjen Biere
  • Wim H. Van der Putten
  • T. Martijn Bezemer
Plant-microbe-animal interactions - Original research


Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.


Aboveground–belowground interactions Induced defense Iridoid glycosides Secondary plant compounds Timing 



We thank Ciska Raaijmakers, Roel Wagenaar, Jinghua Huang, Minghui Fei and Jingying Jing for the technical help and two anonymous reviewers for their helpful comments on a previous version of the manuscript. This work was funded by a grant from the China Scholarship Council (no. 2011630083 to M. G. W.). This is publication no. 5567 of the Netherlands Institute of Ecology (NIOO-KNAW).

Conflict of interest

The authors acknowledge that there are no conflicts of interest and that the experiments comply with the current laws of the Netherlands where the experiments were performed.


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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Minggang Wang
    • 1
  • Arjen Biere
    • 1
  • Wim H. Van der Putten
    • 1
    • 2
  • T. Martijn Bezemer
    • 1
  1. 1.Department of Terrestrial EcologyNetherlands Institute of Ecology (NIOO-KNAW)WageningenThe Netherlands
  2. 2.Laboratory of NematologyWageningen UniversityWageningenThe Netherlands

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