Disentangling the influence of water limitation and simultaneous above and belowground herbivory on plant tolerance and resistance to stress

Authors: MUNDIM, FABIANE - University Of Virginia; VIEIRA-NETO, ERNANE - University Of Florida; Alborn, Hans; BRUNA, EMILIO - University Of Florida

Submitted to: Journal of Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/20/2021
Publication Date: 5/10/2021
Citation: Mundim, F.; Vieira-Neto, E.; Alborn, H.T.; Bruna, E. 2021. Disentangling the influence of water limitation and simultaneous above and belowground herbivory on plant tolerance and resistance to stress. Journal of Ecology. 109:2729–2739. https://doi.org/10.1111/1365-2745.13684.
DOI: https://doi.org/10.1111/1365-2745.13684

Interpretive Summary: A scientist at the chemistry group (USDA ARS CMAVE) in Gainesville FL, in collaboration with colleges at University of Virginia and University of Florida, examined whole-plant tolerance responses of the model plant Solanum lycocarpum to individual and combined effects of above and below ground herbivory under normal water availability and future drought condition as predicted by IPCC studies. By using parameterized generalized linear mixed-effects models we found that plants that experienced normal rain fall, while also challenged with above- and below-ground herbovory (armyworm and root knot nematode), had greater total biomass and lower concentrations of defensive compounds in the leaves than plants exposed solely to root or leaf feeders as well as when compared to the herbivore-free controls, including drought stress control plants. However, drought combined with herbivory resulted in more complex root and foliar chemistry. In addition, nematode root feeding also led to increased total concentrations of terpenoids in leaves relative to controls. In this investigation we found that plant responses to herbivory in variable environments are complex, and that below ground herbivory and damage must be accounted for in the framework of studies of pest tolerance, and that this understanding is essential for a comprehensive understanding of whole-plant responses to stress.

Technical Abstract: Plants face a daily barrage of stressors from the environment, insects, and microorganisms. This is also true for the roots of plants. An ARS scientist at the Center for Medical, Agricultural, and Veterinary Entomology in Gainesville FL, in collaboration with colleagues at the University of Virginia and the University of Florida, examined whole-plant tolerance responses of the plant Solanum lycocarpum, a tropical plant known as wolf apple, to individual and combined effects of above and below ground herbivory (insect and nematode feeding, respectively) under normal water availability as well as under drought conditions. By using models, it was determined that plants that experienced normal rain fall levels and challenged with above- and below-ground herbivory (armyworm and root knot nematode), had greater plant growth and lower concentrations of defensive compounds when compared to plants exposed solely to root or leaf feeders, as well as when compared to the herbivore-free controls, including drought stress control plants. However, drought combined with herbivory resulted in more complex root and foliar chemical compounds. In addition, nematode root feeding also led to increased total concentrations of terpenoids in leaves relative to controls. It was concluded that plant responses to herbivory under variable environments are complex, and that below ground herbivory and damage must be accounted for in the framework of studies of pest tolerance, and that this is essential for a comprehensive understanding of whole-plant responses to stress, particularly for agricultural commodities.