Direct and legacy effects of herbivory on growth and physiology of a clonal plant

Abstract

The ability to tolerate novel herbivores is widely considered to influence plant invasion success. For clonal plants that have reduced capacity to evolve in response to novel herbivores, legacy effects of herbivory on parental plants might be translated to offspring ramets, resulting in pre-adaptation to tolerate herbivory for new vegetative growth. Using the invasive clonal plant Alternanthera philoxeroides, we first exposed plants to herbivory by Planococcus minor, a widespread and generalist piercing-sucking insect. Herbivory decreased above- and below-ground plant biomass by approximately 50% with a concomitant 134% increase in root N concentration but no changes in concentrations of soluble sugars, starch or non-structural carbohydrates related to herbivory tolerance. Offspring ramets were then exposed to herbivory by three different herbivore species: (1) P. minor, (2) the specialist leaf-beetle Agasicles hygrophila, and (3) the stenophagous tortoise-beetle Cassida piperata. There was no evidence of interactive effects between herbivory on parental plants and herbivory on offspring plants on growth, biomass allocation patterns, or physiological responses, suggesting that pre-adaptation to herbivory did not occur in A. philoxeroides with these herbivores. There were, however, species-specific herbivore tolerance responses. In the offspring generation, herbivory by A. hygrophila strongly suppressed growth and biomass allocation, but patterns were generally weaker for other herbivores. Tolerance effects could be explained by stimulatory effects of grazing by C. piperata and P. minor on taproot biomass along with idiosyncratic increases of starch and non-structural carbohydrate concentration in some storage organs. Our results highlight the importance of A. hygrophila in controlling the aboveground spread of A. philoxeroides. However, herbivory by other species was largely tolerated and accompanied by increased allocation to underground storage organs and altered physiological reserves, both of which could allow this invasive plant to tolerate herbivory and successfully invade new areas in the face of new herbivore pressure.

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Acknowledgements

We thank Jia-Hao Wang and Ting Fu for assistance with the management of the experiment and plant harvest, Dr. Bo-Yi Chen, Dr. Jian-Yu Li, and Dr. Yong-Jian Wang for assistance with insect collection, and Qiao-Qi Sun, the associate editor and two anonymous reviewers for their valuable comments. This work was supported by National Key Research and Development Program of China (2016YFC1202102, 2016YFC1201101), National Natural Science Foundation of China (31500331), and Fundamental Research Funds for the Central Universities (2015ZCQ-BH-01).

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Correspondence to Fei-Hai Yu.

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Dong, B., Wang, M., Liu, R. et al. Direct and legacy effects of herbivory on growth and physiology of a clonal plant. Biol Invasions 20, 3631–3645 (2018). https://doi.org/10.1007/s10530-018-1801-5

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Keywords

  • Alternanthera philoxeroides
  • Generalist and specialist herbivores
  • Herbivore type
  • Maternal effect
  • Nitrogen
  • Non-structural carbohydrates