Herbivory induces both direct and indirect defenses in plants; however, some combinations of these defenses may not be compatible. The jasmonate signal cascade activated both direct (nicotine accumulations) and indirect (mono- and sesquiterpene emissions) whole-plant defense responses in the native tobacco Nicotiana attenuata Torr. Ex Wats. Nicotine accumulations were proportional to the amount of leaf wounding and the resulting increases in jasmonic acid (JA) concentrations. However, when larvae of the nicotine-tolerant herbivore, Manduca sexta, fed on plants or their oral secretions were applied to leaf punctures, the normal wound response was dramatically altered, as evidenced by large (4- to 10-fold) increases in the release of (i) volatile terpenoids and (ii) ethylene, (iii) increased (4- to 30-fold) accumulations of endogenous JA pools, but (iv) decreased or unchanged nicotine accumulations. The ethylene release, which was insensitive to inhibitors of induced JA accumulation, was sufficient to account for the attenuated nicotine response. Applications of ethylene and ethephon suppressed the induced nicotine response and pre-treatment of plants with a competitive inhibitor of ethylene receptors, 1-methylcyclopropene, restored the full nicotine response. This ethylene burst, however, did not inhibit the release of volatile terpenoids. Because parasitoids of Manduca larvae are sensitive to the dietary intake of nicotine by their hosts, this ethylene-mediated switching from direct to a putative indirect defense may represent an adaptive tailoring of a plant's defense response.

Theory on costs of plant defense against herbivory in stressful environments predicts that costs should increase when competition is intense. This amplifies a fundamental dilemma that plants are thought to face: allocate limited resources to grow fast enough to compete, or invest these resources in secondary metabolites to maintain defense. We studied costs associated with genetic and environmental variation in secondary metabolite production of Brassica rapa in the presence and absence of the generalist competitor Lolium perenne. We used experimental quantitative genetics (artificial selection) to manipulate genetic variation, and herbivore-induction treatments to produce environmental variation in myrosinase and glucosinolate concentrations and resistance. Glucosinolates, and their byproducts after breakdown by myrosinase, are known to affect herbivory on plants in the Brassicaceae family. Defense costs were significant in the absence of competitors, but in contrast to theoretical predictions, costs of constitutive defense (measured as growth rates) were not detectable and the cost of induced defense remained the same in the competitive environment. To understand what factors made constitutive defense costs not detectable under competition we conducted several experiments to assess the effects of limited resources and allelopathy on costs and benefits of the defense chemicals. None of the experiments involving nutrient supply and weak competition supported the hypothesis that the lack of defense costs in competitive environments was due to limited resources. Instead, the breakdown products of the glucosinolate-myrosinase reaction appeared to function as allelopathic agents, which may benefit B. rapa plants in competition, thereby reducing net costs of chemical defense. We found that: (1) the effects of exogenous glucosinolates on Lolium root length depended on the presence of myrosinase. (2) In the absence of nutrients, Lolium root lengths were shorter when seeds germinated with B. rapa. (3) Genetic increases in glucosinolate concentration negatively affected Lolium seedling growth only when there were simultaneous genetic increases in myrosinase concentration. Activated carbon treatments designed to neutralize allelopathic effects and restore costs in the competitive environments were, however, not statistically significant. When plant defenses also function to benefit plants in competitive interactions, plants may evolve to compete and defend.

Changes in herbivory and resource availability during a plant's development should promote ontogenetic shifts in resistance and tolerance, if the costs and benefits of these basic strategies also change as plants develop. We proposed and tested a general model to detect the expression of ontogenetic tradeoffs for these two alternative anti-herbivory strategies in Raphanus sativus. We found that ontogenetic trajectories occur in both resistance and tolerance but in opposite directions. The juvenile stage was more resistant but less tolerant than the reproductive stage. The ontogenetic switch from resistance to tolerance was consistent with the greater vulnerability of young plants to leaf damage and with the costs of resistance and tolerance found at each stage. We posit that the ontogenetic perspective presented here will be helpful in resolving the current debate on the existence and detection of a general resistance-tolerance tradeoff.

Defense costs provide a major explanation for why plants in nature have not evolved to be better defended against pathogens and herbivores; however, evidence for defense costs is often lacking. Plants defend by deploying resistance traits that reduce damage, and tolerance traits that reduce the fitness effects of damage. We first tested the defense-stress cost (DSC) hypothesis that costs of defenses increase and become important under competitive stress. In a greenhouse experiment, uniparental maternal families of the host plant Arabis perennans were grown in the presence and absence of the bunch grass Bouteloua gracilis and the herbivore Plutella xylostella. Costs of resistance and tolerance manifest as reduced growth in the absence of herbivory were significant when A. perennans grew alone, but not in the competitive environment, in contrast to the DSC hypothesis. We then tested the defense-stress benefit (DSB) hypothesis that plant defenses may benefit plants in competitive situations thereby reducing net costs. For example, chemical resistance agents and tolerance may also have functions in competitive interactions. To test the DSB hypothesis, we compared differentially competitive populations for defense costs, assuming that poorer competitors from less dense habitats were less likely to have evolved defenses that also function in competition. Without competitive benefits of defenses, poorer competitors were expected to have higher net costs of defenses under competition in accordance with DSB. Populations of A. perennans and A. drummondii that differed dramatically in competitiveness were compared for costs, and as the DSB hypothesis predicts, only the poor competitor population showed costs of resistance under competition. However, cost of tolerance under competition did not differ among populations, suggesting that the poor competitors might have evolved a general stress tolerance. Although the DSC hypothesis may explain cases where defense costs increase under stress, the DSB hypothesis may explain some cases where costs decrease under competitive stress.