Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta

Abstract

Many plants employ induced responses against generalist herbivores. Specialist herbivores, however, may employ several mechanisms to overcome the negative effects of induced plant defenses. Here we test how the behavior and development of specialist Manduca sexta larvae are affected by induced responses in their natural host plant Nicotiana attenuata. On a spatial scale relevant to both the plant and the herbivore, we first determined how methyl jasmonate (MeJA)-induced responses, such as increased nicotine production, affect the tendency of larvae to leave induced plants. When larvae were allowed to move between two plants planted in one pot, they left an MeJA-treated plant faster than a control plant. When both plants in the pot were MeJA-treated, the larvae developed more slowly than when both plants were uninduced, or when the larvae had the opportunity to move to an uninduced neighbor. The sooner larvae moved from an MeJA-treated plant to an untreated neighbor, the larger the body mass they attained. This demonstrates that M. sexta larvae can compensate behaviorally for the deleterious effects of induced plant responses. These effects were observed in plants grown under both low and high N supply rates, though the effects were more pronounced under high N. To examine the consequences of the timing and the direction of the host plant switching behavior for larval development, neonate larvae were fed leaves excised from induced and uninduced plants. Larvae confined to MeJA-treated leaves had higher mortality rates and grew slower than larvae fed only control leaves. This demonstrates that MeJA-induced responses decrease growth and development of specialist herbivores that do not have the behavioral option of moving to an uninduced plant. The sooner the larvae were switched to MeJA-treated leaves, the slower their development compared to larvae fed only uninduced leaves. In contrast, the sooner larvae fed MeJA-treated leaves were switched to control leaves, the faster they developed. Again the effects of MeJA treatment were stronger in plants grown under high N supply. We propose that induced plants growing in close competition with an uninduced conspecific may offset the fitness costs of these induced responses and perhaps obtain a fitness benefit by motivating herbivores to move to their neighboring competitors.

Population genetic structure of two primary parasitoids of Spodoptera frugiperda (Lepidoptera), Chelonus insularis and Campoletis sonorensis (Hymenoptera): to what extent is the host plant important?

“…Insect pests are directly targeted by plant toxic secondary compounds (Giamoustaris & Mithen 1995;van Dam et al 2000;Rausher 2001;van Dam 2009) and they have evolved various strategies to circumvent plant defense mechanisms (Futuyma 1983;Nitao 1989;Berenbaum & Zangerl 1992;Evans et al 2000;Ode et al 2004;Zhu-Salzman & Zeng 2008). Because of the intimate trophic interactions between immature parasitoids and their hosts, plant chemistry also indirectly affects the fitness of parasitoids (Bottrell et al 1998;Turlings & Benrey 1998).…”

Development of an Insect Herbivore and its Pupal Parasitoid Reflect Differences in Direct Plant Defense

“…Most plants also produce secondary metabolites that affect herbivore behavior and development. Allelochemicals may function as feeding deterrents for generalist herbivores (Akhtar and Isman 2004) or exhibit toxic effects on the development and physiology of herbivores by reducing their rates of growth and increasing mortality Wold and Marquis 1997;van Dam et al 2000). On the other hand, many herbivores have evolved specific metabolic adaptations that enable them to detoxify or excrete allelochemicals and their breakdown products (Ratzka et al 2002;Wittstock et al 2004).…”

“…Biotic selection pressures, such as attack from herbivores and pathogens, and abiotic selection pressures, such as exposure to wind or access to water and nutrients, may play an important role in shaping the evolution of direct defenses in plants (Agrawal 2005). Competition with other plants may also be an important factor resulting in a trade-off between growth and defense (van Dam et al 2000).…”

“…This approach has generally argued that natural enemies, by regulating herbivore populations, can act as important selective agents by reducing the need for plants to invest in chemical defenses when these are costly to maintain (van Dam et al 2000;Ode et al 2004). However, one of the major problems with this argument is that it assumes that the development of natural enemies is independent of plant quality, thus ignoring that natural enemies obtain their nutrition indirectly from the plant through the herbivore.…”

Analyzing plant defenses in nature

“…16 Defenses mediated by secondary plant compounds are generally believed not to affect specialist herbivores, because of their capacity to tolerate or to detoxify defensive compounds of their hosts by behavioral or physiological adaptations. [17][18][19][20] In this context, the specialist herbivore paradigm predicts that adapted herbivores are less affected by a given chemical defense than generalists, 21,22 although exceptions have been noted. [23][24][25] While it is important to consider these numerous sources of variation affecting the outcome of herbivore-plant interactions when designing functional studies, a significant fraction of the function of cyanogenesis in nature.…”