“Delayed chemical defense: timely expulsion of herbivores reduces competition with neighboring plants”

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Pia Backmann, Volker Grimm, Gottfried Jetschke, Yue Lin, Matthijs Vos, Ian T. Baldwin, and Nicole M. van Dam (Jan 2019)

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Modeling shows that plants may use their herbivores to weaken competitors by delaying their defense reaction

Slow can be good – as long as you put up your defenses in time

When a plant is attacked by a larva, it has two ways to react. It may produce defense compounds immediately (A) and, as a consequence, grow slower than its neighbors. Alternatively, it may continue growing without producing defense. In that case, the insect continues feeding, and the plant loses a large amount of biomass (B). This dilemma is called “growth-defense trade-off.”
(Figure made by Pia Backmann)

A plant faces several challenges in its life. It competes with neighboring plants for nutrients. At the same time, herbivores, such as caterpillars, want to eat it. Plants use chemical defenses to defend themselves against attackers. However, producing defense toxins is costly and slows the plant’s growth. Neighbors can easily outgrow a highly defended plant. Therefore, many plants use inducible defenses and produce defenses upon attack as a cost-saving strategy. However, there is a delay between the insect’s first bite and the plant’s defense response. In this time period, the plant is undefended and suffers feeding damage. Consequently, scientists had always assumed that natural selection should prefer small delay times.

The authors of this study challenged this idea. This was motivated by the observation that caterpillars eat very little when they are small, whereas they consume 90% of all they eat in their entire lifetime in the last days before pupation. Therefore, it might be better to keep the small caterpillars. When they grow larger, and become more damaging, the defense should kick in. At that time, the plant should send the voracious caterpillar off – like a missile – to the neighbors.

Left, Nicotiana attenuata, the studied plant species in its natural habitat. Right, Manduca sexta feeding on a tobacco plant.
(Photos: Pia Backmann)

To explore this idea, the authors developed an individual-based model (Backmann, Grimm, Lin). They used experimental data from wild tobacco, Nicotiana attenuata, and its specialized herbivore, Manduca sexta from the lab (van Dam) and the field (Backmann, Baldwin). Using this model, the authors found that under strong competition and high herbivore pressure, the most efficient delay times were synchronized with the time the larvae need to grow large enough to severely damage neighboring plants. Based on this the authors concluded that being slow can be good, if the reaction is well-timed.

View of the great Basin Desert, habitat of the study plant, the wild tobacco, Nicotiana attenuata. Photo taken at the Field station of the Max Planck Institute for Chemical Ecology at Brigham Young University’s Lytle Ranch Preserve in southwest Utah.
(Photo: Danny Kessler)


Time delays in plant responses to insect herbivory are thought to be the principal disadvantage of induced over constitutive defenses, suggesting that there should be strong selection for rapid responses. However, observed time delays between the onset of herbivory and defense induction vary considerably among plants. We postulate that strong competition with conspecifics is an important co-determinant of the cost-benefit balance for induced responses. There may be a benefit to the plant to delay mounting a full defense response until the herbivore larvae are mobile enough to leave, and large enough to cause severe damage to neighboring plants. Thus, delayed responses could reduce the competitive pressure on the focal plant. To explore this idea, we developed an individual-based model using data from wild tobacco, Nicotiana attenuata, and its specialized herbivore, Manduca sexta. Chemical defense was assumed to be costly in terms of reduced plant growth. We used a genetic algorithm with the plant’s delay time as a heritable trait. A stationary distribution of delay times emerged, which under high herbivore densities peaked at higher values, which were related to the time larvae need to grow large enough to severely damage neighboring plants. Plants may thus tip the competitive balance by expelling insect herbivores to move to adjacent plants when the herbivores are most damaging. Thereby herbivores become part of a plant’s strategy for reducing competition and increasing fitness.