Meta-Analysis of Sources of Variation in Fitness Costs of Plant Antiherbivore Defenses

Abstract

Plant defense theories predict that allocation to antiherbivore defenses should impose a cost on plants, manifested as a reduction in growth and reproduction. However, the empirical evidence for the existence of such trade-offs is conflicting, suggesting that significant fitness costs of defense arise in some circumstances but not in others. A meta-analysis of 70 studies assessing the relationship between measures of plant defense and growth or reproduction has been conducted to examine the relative importance of several potential sources of variation in the fitness costs of defense. The magnitude of fitness costs varied depending on whether they were measured at the level of phenotype or genotype. The mean magnitude of among-genotype correlations (AGCs) between defense and fitness measures (r = −0.30) was higher than that of among-phenotype correlations (APCs; r = −0.15). Moreover, AGCs tended to be more negative when defense was assessed as the inverse of herbivore densities or damage rather than in terms of single specific chemical or structural traits. The magnitude of APCs was greatly influenced by environmental variation; phenotypic costs were lowest under controlled experimental conditions and highest in studies that minimized genetic variation among plants. In addition, the magnitude and sign of APCs varied depending on nutrient availability and the type of defensive compound. APCs were negative at high levels of nutrient availability and for defenses associated with alkaloids and phenolics but tended to be positive at low levels of nutrient availability and for defenses associated with terpenoids. In contrast, the magnitude of fitness costs was not significantly affected by the presence of herbivores, type of plant, type of defense (constitutive, mechanical, or induced), concentrations of defensive compounds, or measure of plant fitness. The above patterns of variation in the magnitude of correlations between defense and fitness measures are inconsistent with the notion that fitness costs are incurred through diversion of common limited resources from growth and reproduction to defense (allocation costs). Instead, the prevalence of significant negative correlations under uncontrolled environmental conditions and their persistence in the presence of herbivores both imply that fitness costs of defense may often arise through interactions between plants and their abiotic and biotic environment (competitors, pollinators, different types of herbivores, their natural enemies, and various types of abiotic stresses). Because the above aspects have usually been excluded in studies aiming at detecting internal allocation trade-offs, the failure to detect costs in some cases may be a consequence of the experimental design. Future studies should examine the relative importance of opportunity and ecological types of costs by manipulating various aspects of plant environment.