Quantifying a trait-mediated indirect effect of an environmental stressor on predator-prey dynamics

Trait-mediated indirect interactions have been intensively studied to understand ecological dynamics in biological communities. Yet, little is known about the relative importance of trait-mediated indirect effects of environmental stressors on population dynamics. How does an environmental stressor indirectly affect the population dynamics of a focal species by altering the traits of interacting species and the strength of interspecific interactions? Here, we quantified the direct and trait-mediated indirect effects of an environmental stressor by combining rotifer-alga experiments and Bayesian parameter estimation of a dynamic model. These days, human activities salinize freshwater lakes globally, thereby increasing the death rates and decreasing birth rates of plankton species. Salinity stress is also known to induce cell clumping in certain phytoplankton species. As larger clumps work as a defense trait against gape-limited predation by zooplankton, the salinity stress can affect zooplankton not only directly but also indirectly through phytoplankton trait changes. We first show that a green alga, Chlamydomonas sphaeroides , formed larger clumps than the two model species of green algae ( Chlamydomonas reinhardtii and Chlorella vulgaris ) under a moderate salinity stress (0.06M NaCl). Then, by tracking the clump size distributions of Chlamydomonas sphaeroides , we confirmed that small clumps are more vulnerable to predation by rotifers, Brachionus calyciflorus , as previous studies demonstrated. Finally, we co-cultured the green algae and rotifers for a week with and without salinity stress and fitted the Lotka-Volterra predator-prey model. We first estimated how salinity stress increased the rotifer mortality rate using Chlorella vulgaris , which seldom showed clump formation. Then, by using Chlamydomonas sphaeroides , we estimated how salinity stress increased the mortality rate and decreased the attack rate due to clump formation. We found that salinity stress increased the rotifer mortality rate by more than seventeen-fold, and decreased the attack rate on Chlamydomonas sphaeroides to approximately half of that without salinity stress. These results indicate that salinity stress can weaken the predator-prey interaction, and thus salinization can harm freshwater zooplankton species through increasing the mortality rates and decreasing the attack rates. This will be an important step for a quantitative understanding of how environmental stressors can affect community dynamics via trait modifications.