Plant defence theory re‐examined: nonlinear expectations based on the costs and benefits of resource mutualisms

Abstract

Summary 1. General theories of plant defence often fail to account for complex interactions between the resources required for defence expression. For example, the carbon that is used for carbon‐based defence is acquired using nutrient‐rich photosynthetic pigments, while nutrient gain itself requires substantial carbon allocation belowground. We should therefore expect the expression of plant defence to reflect the tight linkage between carbon and nutrient gain, yet mechanistic studies linking resource gain with plant defence theory have been slow to emerge. 2. The overwhelming majority of plants participate in nutrition mutualisms with fungal or bacterial symbionts. We propose the resource exchange model of plant defence (REMPD) in which the costs and benefits associated with nutrition mutualisms affect plant resource status and allocation to growth and defence. The model predicts quadratic relationships between mutualist abundance and expression of defence. Within plant genotypes, both plant biomass and defence expression are maximized at optimal nutrient exchange among mutualistic partners, and as a consequence, the two are positively associated. 3. We tested the model by growing Asclepias syriaca, the common milkweed, with two mycorrhizal fungal species in nine fungal abundance treatments. Plant growth and defence traits and mycorrhizal colonization were quantified after 14 weeks of plant growth. Linear, quadratic, saturating and exponential decay models were fit to curves relating the proportion of root colonized by mycorrhizal fungi to plant traits, and compared using AICc. 4. As predicted by our model, increasing colonization by Scutellospora pellucida produced quadratic responses in plant growth, latex exudation and cardenolide production. In contrast, Glomus etunicatum appeared to act as a parasite of A. syriaca, causing exponential decline in both plant growth and latex exudation. As predicted by our model, plant growth was positively correlated with all defences quantified. 5. Synthesis. The REMPD combines cost–benefit analysis of mutualisms with plant resource acquisition strategies to predict the expression of plant defence. The effects of S. pellucida and G. etunicatum on defence expression differ; however, both provide support for the model and suggest that resource mutualisms affect the expression of defence in a predictable nonlinear fashion.