Concerted effects of direct and indirect plant defenses in nature: A case study using lima bean (Phaseolus lunatus L.)

Background/Question/Methods

Indirect plant defenses against herbivorous insects function via the attraction of arthropod carnivores. The result of this interaction is considered beneficial for the plant as herbivore pressure is reduced and, ultimately, plant fitness is increased. Under natural conditions, we tested whether induced plant defenses provide a benefit to plants. Using lima bean (Phaseolus lunatusL.), we induced the secretion of extrafloral nectar (EFN) with jasmonic acid—a natural plant hormone centrally involved in the induction of indirect defenses (i.e., VOCs; volatile organic compounds and EFN). EFN attracts mainly ants that are thought to deter herbivores with their mere presence or by preying on them. To account for the complexity of natural systems, we introduced another level of variability by using three high cyanogenic (HC) and three low cyanogenic (LC) lima bean genotypes. Cyanogenesis is the wound induced release of hydrogen cyanide from preformed precursors in response to cell damage and represents a constitutive direct defense. This experimental setup enabled us to test the concerted effects of cyanogenesis and  EFN on higher trophic levels and the resulting effects for plants.

Results/Conclusions

We found a tradeoff between cyanogenesis (direct, constitutive defense) and an indirect, inducible defense (EFN) as induced LC genotypes showed a significantly higher secretion of EFN than induced HC genotypes. Analyzes of fitness relevant growth parameters showed that HC plants (low EFN) developed slower and had less biomass than LC plants (high EFN) indicating higher costs through nitrogen-based cyanogenesis than through mainly carbon-based EFN and VOCs. However, induced plants of each cyanotype (LC or HC) were shorter and accumulated less biomass than controls of the same cyanotype indicating additional costs of indirect defense. Enhanced EFN production quantitatively attracted ants from the vicinity, but all plants were visited by ants. Induced LC plants with the highest amounts of EFN, had more ant activity, and less damage due to herbivory through chewing insects as non-induced controls. However, ants of one dolichoderine species (Dorymyrmex sp.) dominated the ant communities and led to increased numbers of aphids on these plants. Our study illustrates that induced defenses are less costly than cyanogenesis, but can have vastly different outcomes for plants as various predators and herbivores are differentially affected.