Two-tiered defense strategy may compensate for predator avoidance costs of an ecosystem engineer

Inducing defenses to deter predators is a necessary process theorized to incur costs. Although studies have investigated defense trade-offs, quantifying trade-offs is challenging and costs are often inferred. Additionally, prey employ strategies to reduce costs, making costs difficult to predict. Our purpose was to investigate induced defense costs by characterizing the defense mechanisms and costs in eastern oysters (Crassostrea virginica). In the field, newly-settled oysters exposed to blue crab (Callinectes sapidus) exudates grew stronger shells containing less percent organic material than oysters in controls. In natural populations, shell density was negatively correlated with shell thickness, further suggesting oysters thicken their shells by increasing low-density calcium carbonate. Reproductive investment showed an increasingly negative relationship with thickness as density decreased (and induction increased). In a laboratory experiment, oysters exposed to a temporal gradient in risk grew heavier shells in all crab treatments, but only grew stronger shells under constant exposure. Collectively, these results suggest oysters initially react to predators by adding inexpensive calcium carbonate to their shells to quickly outgrow risk. However, in high-risk environments, oysters may increase the production of costly organic material to increase the shell strength. Thus, oysters demonstrate a two-tier mechanism allowing them to cheaply escape predation at lower risk but to build stronger shells at greater expense when warranted. These results illuminate the complex strategies prey deploy to balance predation risk and defense costs as well as the importance of understanding these strategies to accurately predict predator effects.