Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability : Costs of constitutive and induced pine tree defences

Several hypotheses, mainly Optimal Defense (OD), Carbon: Nutrient Balance (CNB), Growth Rate (GR), and Growth-Differentiation Balance (GDB), have individually served as frameworks for investigating the patterns of plant defense against herbivores, in particular the pattern of constitutive defense. The predictions and tests of these hypotheses have been problematic for a variety of reasons and have led to considerable confusion about the state of the "theory of plant defense." The primary contribution of the OD hypothesis is that it has served as the main framework for investigation of genotypic expression of plant defense, with the emphasis on allocation cost of defense. The primary contribution of the CNB hypothesis is that it has served as the main framework for investigation of how resources affect phenotypic expression of plant defense, often with studies concerned about allocation cost of defense. The primary contribution of the GR hypothesis is that it explains how intrinsic growth rate of plants shaped evolutionarily by resource availability affects defensive patterns. The primary contribution of the expanded GDB hypothesis is that it recognizes the constant physiological tradeoff between growth and differentiation at the cellular and tissue levels relative to the selective pressures of resource availability, including explicitly taking into account plant tolerance of damage by enemies. A clearer understanding of these hypotheses and what we have learned from investigations that use them can facilitate development of well-designed experiments that address the gaps in our knowledge of plant defense.

Given that a plant's defensive strategy against herbivory is never likely to be a single trait, we develop the concept of plant defense syndromes, where association with specific ecological interactions can result in convergence on suites of covarying defensive traits. Defense syndromes can be studied within communities of diverse plant species as well as within clades of closely related species. In either case, theory predicts that plant defense traits can consistently covary across species, due to shared evolutionary ancestry or due to adaptive convergence. We examined potential defense syndromes in 24 species of milkweeds (Asclepias spp.) in a field experiment. Employing phylogenetically independent contrasts, we found few correlations between seven defensive traits, no bivariate trade-offs, and notable positive correlations between trichome density and latex production, and between C:N ratio and leaf toughness. We then used a hierarchical cluster analysis to produce a phenogram of defense trait similarity among the 24 species. This analysis revealed three distinct clusters of species. The defense syndromes of these species clusters are associated with either low nutritional quality or a balance of higher nutritional quality coupled with physical or chemical defenses. The phenogram based on defense traits was not congruent, however, with a molecular phylogeny of the group, suggesting convergence on defense syndromes. Finally, we examined the performance of monarch butterfly caterpillars on the 24 milkweed species in the field; monarch growth and survival did not differ on plants in the three syndromes, although multiple regression revealed that leaf trichomes and toughness significantly reduced caterpillar growth. The discovery of convergent plant defense syndromes can be used as a framework to ask questions about how abiotic environments, communities of herbivores, and biogeography are associated with particular defense strategies of plants.