The Chemistry of Defense and Apparency in the Corollas OfNicotiana Attenuata

The morphological and chemical characteristics of flowers which attract pollinators present a dilemma for plants; advertising may increase the "apparency" of plants to their predators and some pollinators are also predators. We explore how a self-compatible disturbance species,Nicotiana attenuata, copes with this potential dilemma by examining the changes in emission of chemicals from flowers in response to pollination and herbivory. We propose that chemical changes induced by herbivory and pollination reflect the function of the chemicals in the plant. The emission of a single compound, benzyl acetone (BA, 4-phenyl-2-butanone), by flowers increases dramatically (50x) in the evening, peaking just after dark -a pattern of emission characteristic of moth-pollinated flowers. Pools of BA were found only in the outer lip of the corolla where pollinators come in contact with the flower, and diurnal changes in the size of the corolla pool closely paralleled the amount emitted by intact flowers throughout the day, as determined by headspace sampling. Pollination dramatically decreases both the pools of BA in the corolla and its emission from flowers. Similarly, nicotine, a broadly biocidal defense metabolite and an induced defense in vegetative and reproductive tissues, is also found in the headspace of flowers and is principally localized in the basal parts of the corolla below the attachment of the filaments and the nectar reward. Moreover, the dynamics of the corolla pools of BA and nicotine throughout the day are consistent with their roles in advertisement and defense, respectively. The corolla pools of nicotine are stable throughout the day except during the period of peak BA production and emission when nicotine pools decrease significantly. The coordinated increase in BA emission and decline in nicotine pools are not inexorably linked, because herbivory or mechanical damage to corolla tissue rapidly increases corolla nicotine pools without affecting the increase in BA pools. Similarly, leaf damage results in a slower, systemic increase in corolla nicotine pools during reproductive growth but again does not affect BA pools. Excised flowers emitted BA in a manner similar to that of intact flowers, and excision of a majority of flowers from a plant did not alter the BA emission patterns of the remaining flowers. We conclude that althoughN. attenuata's defensive and advertisement chemistries respond synchronously to some environmental stimuli, the flowers' chemical responses to pollinators and herbivoresare distinct and the differences reflect their ecological roles. We propose that the cost-benefit framework of the optimal defense and apparency theories can be fruitfully applied to the allocation of defense metabolites and floral volatiles that function in pollinator attraction, and that this framework can be readily tested by manipulating the patterns of the emissions of plants in the field.