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Functional interactions in the use of direct and indirect defences in native Nicotiana plants.

Nicotiana attenuata has both direct (induced nicotine production) and indirect (induced release of mono- and sesquiterpenes) defences induced by herbivore attack; both are activated by the jasmonate cascade, albeit in different tissues (roots and shoots, respectively). The fact that both types of defences are induced suggests that their benefits are conditional. Indeed, jasmonate treatment of roots to induce nicotine production increases plant fitness correlates (lifetime viable seed production) when plants are grown in environments with herbivores, but decreases fitness when they are not. Because inducing nicotine production can make 6% of a plant's nitrogen budget unavailable for seed production, it can exact a resource-based cost. Volatile production is likely to be less costly but could make plants more 'apparent' to herbivores and thereby exact an ecological cost. Direct defences could also have ecological costs if they are sequestered by specialist herbivores and used against their enemies. Herbivory by the nicotine-tolerant herbivore Manduca sexta dramatically amplifies the increase in jasmonates and the quantity of volatiles released, but decreases the nicotine response in comparison to mechanical simulations of the wounding that larval feeding causes. The apparent switching from nicotine production to the release of volatiles may reflect incompatibilities in the use of direct and indirect defences with specialist herbivores.