Above–Belowground Herbivore Interactions in Mixed Plant Communities Are Influenced by Altered Precipitation Patterns

Abstract

Root- and shoot-feeding herbivores have the capacity to influence one another by modifying the chemistry of the shared host plant. This can alter rates of nutrient mineralization and uptake by neighboring plants and influence plant–plant competition, particularly in mixtures combining grasses and legumes. Root herbivory-induced exudation of nitrogen (N) from legume roots, for example, may increase N acquisition by co-occurring grasses, with knock-on effects on grassland community composition. Little is known about how climate change may affect these interactions, but an important and timely question is how will grass–legume mixtures respond in a future with an increasing reliance on legume N mineralization in terrestrial ecosystems. Using a model grass–legume mixture, this study investigated how simultaneous attack on lucerne (Medicago sativa) by belowground weevils (Sitona discoideus) and aboveground aphids (Acyrthosiphon pisum) affected a neighboring grass (Phalaris aquatica) when subjected to drought, ambient, and elevated precipitation. Feeding on rhizobial nodules by weevil larvae enhanced soil water retention under ambient and elevated precipitation, but only when aphids were absent. While drought decreased nodulation and root N content in lucerne, grass root and shoot chemistry were unaffected by changes in precipitation. However, plant communities containing weevils but not aphids showed increased grass height and N concentrations, most likely associated with the transfer of N from weevil-attacked lucerne plants containing more nodules and higher root N concentrations compared with insect-free plants. Drought decreased aphid abundance by 54% but increased total and some specific amino acid concentrations (glycine, lysine, methionine, tyrosine, cysteine, histidine, arginine, aspartate, and glutamate), suggesting that aphid declines were being driven by other facets of drought (e.g., reduced phloem hydraulics). The presence of weevil larvae belowground decreased aphid numbers by 30%, likely associated with a significant reduction in proline in weevil-treated lucerne plants. This study demonstrates how predicted changes to precipitation patterns and indirect interactions between herbivores can alter the outcome of competition between N-fixing legumes and non-N-fixing grasses, with important implications for plant community structure and productivity.

Climate and atmospheric change impacts on sap‐feeding herbivores: a mechanistic explanation based on functional groups of primary metabolites

“…Other climate change factors, including changes in rainfall patterns (e.g. drought), have been shown to alter N dynamics, amino acid concentrations and aphid populations within the same system (Ryalls et al 2016b). It is therefore likely that water stress will interact with plant and aphid responses to eT and eCO 2 .…”

Silicon‐induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance

“…Johnson, Ryalls & Karley ; Ryalls et al . ). Silicon supplantation may therefore indirectly promote the performance of some herbivores if it causes such changes in the host plant.…”

Production of pyrrolizidine alkaloids and shikonins in Echium plantagineum L. in response to various plant stressors

“…As plants are sessile and have typically coexisted with herbivores and other pests such as weeds and pathogens for millions of years, the evolution of highly specialized defense mechanisms, including the production or expression of chemical defenses, has typically resulted in enhanced survival rates . Higher plants successfully adapt to moderate environmental stresses including pest infestation using a variety of mechanisms, which are physical and biochemical and in many cases employ both for enhanced survival . Exotic species also demonstrate numerous stress defense mechanisms, but in some cases these mechanisms may not fully protect the plant from environmental pressures not previously encountered .…”

“…). Moderate drought stress, however, significantly reduced the accumulation of selected PAs, possibly due to the additional energy directed towards biosynthesis of NQs and their related precursors . Decreased abundance and downregulation of PAs under moderate drought conditions would likely render plants subjected to non‐herbivore stressors less well defended from herbivore attacks due to lower accumulation of such bioactive PAs …”

“…Constitutive expression of PAs was likely impacted by the decrease in availability of resources as shifts in carbon resources to the roots occurred in association with NQ production (Fig. ) . Additionally, increase in NQ concentrations following stress treatment suggests rapid upregulation of genes associated with biosynthesis in the roots and a local abundance of associated precursors providing a carbon reservoir.…”