Ecological interactions shape the adaptive value of plant defence: Herbivore attack versus competition for light

Abstract

Plants defend themselves against diverse communities of herbivorous insects. This requires an investment of limited resources, for which plants also compete with neighbours. The consequences of an investment in defence are determined by the metabolic costs of defence as well as indirect or ecological costs through interactions with other organisms. These ecological costs have a potentially strong impact on the evolution of defensive traits, but have proven to be difficult to quantify. We aimed to quantify the relative impact of the direct and indirect or ecological costs and benefits of an investment in plant defence in relation to herbivory and intergenotypic competition for light. Additionally, we evaluated how the benefits of plant defence balance its costs in the context of herbivory and intergenotypic competition. To this end, we utilised a functional‐structural plant (FSP) model of Brassica nigra that simulates plant growth and development, morphogenesis, herbivory and plant defence. In the model, a simulated investment in defences affected plant growth by competing with other plant organs for resources and affected the level and distribution of herbivore damage. Our results show that the ecological costs of intergenotypic competition for light are highly detrimental to the fitness of defended plants, as it amplifies the size difference between defended and undefended plants. This leads to herbivore damage counteracting the effects of intergenotypic competition under the assumption that herbivore damage scales with plant size. Additionally, we show that plant defence relies on reducing herbivore damage rather than the dispersion of herbivore damage, which is only beneficial under high levels of herbivore damage. We conclude that the adaptive value of plant defence is highly dependent on ecological interactions and is predominantly determined by the outcome of competition for light. plain language summary is available for this article.

Plant ontogeny determines strength and associated plant fitness consequences of plant‐mediated interactions between herbivores and flower visitors

“…For annual plants, the main defence strategy early in plant development is resistance, while later in plant development this switches to tolerance (Boege et al, ). Increased investment of black mustard in resistance and loss of important photosynthetic tissues due to herbivore damage early in life will be especially expensive (de Vries et al, , ). This can explain our observed reduction in flowers, the number of seeds produced and seed weight for plants exposed in the vegetative stage to P. brassicae caterpillars or B. brassicae aphids.…”

“…Second, investment in one component may alter plant interactions with other community members (de Vries, Evers, & Poelman, ; Dutton, Luo, Cembrowski, Shore, & Frederickson, ; Lucas‐Barbosa, ; Villamil, ). For example, large plants may be more apparent to herbivores as a result of increased investment in growth induced by competition for light (de Vries, Evers, Dicke, & Poelman, ). Plant defence responses to herbivory can affect plant reproduction by changes in flowering time, flower abundance and plant interactions with flower visitors (Rusman, Lucas‐Barbosa, Poelman, & Dicke, ).…”

Ecological significance of light quality in optimizing plant defence

“…First, the advantage of a defence gradient is expected to become even stronger when insect herbivores prefer to feed on young leaves near the tip of the branches. Second, the gradient in leaf defence expression within a canopy as established by R:FR can benefit the plant by dispersing herbivore damage away from young leaves (Cipollini et al, ), which is shown to benefit plants in competition with conspecifics, but only under high herbivore pressure (de Vries, Evers, Dicke, & Poelman, ; de Vries, Poelman, et al, ). If this effect would have been included in this study, it would have resulted in a bigger advantage of R:FR‐mediated defence.…”

Cell Communications among Microorganisms, Plants, and Animals: Origin, Evolution and Interplays

“…allowing information sharing and communication between them [193]. This sharing may be favorable despite the cost of alarm signaling toward potential competitor species [194]. Indeed, it allows cooperation in herbivore insect exclusion from their common neighborhood through herbivoreinduced plant volatile molecules acting via epigenetic mechanisms that sustain the memorization of the defense response [195].…”