Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem

In coastal marine food webs, small invertebrate herbivores (mesograzers) have long been hypothesized to occupy an important position facilitating dominance of habitat-forming macrophytes by grazing competitively superior epiphytic algae. Because of the difficulty of manipulating mesograzers in the field, however, their impacts on community organization have rarely been rigorously documented. Understanding mesograzer impacts has taken on increased urgency in seagrass systems due to declines in seagrasses globally, caused in part by widespread eutrophication favoring seagrass overgrowth by faster-growing algae. Using cage-free field experiments in two seasons (fall and summer), we present experimental confirmation that mesograzer reduction and nutrients can promote blooms of epiphytic algae growing on eelgrass (Zostera marina). In this study, nutrient additions increased epiphytes only in the fall following natural decline of mesograzers. In the summer, experimental mesograzer reduction stimulated a 447% increase in epiphytes, appearing to exacerbate seasonal dieback of eelgrass. Using structural equation modeling, we illuminate the temporal dynamics of complex interactions between macrophytes, mesograzers, and epiphytes in the summer experiment. An unexpected result emerged from investigating the interaction network: drift macroalgae indirectly reduced epiphytes by providing structure for mesograzers, suggesting that the net effect of macroalgae on seagrass depends on macroalgal density. Our results show that mesograzers can control proliferation of epiphytic algae, that top-down and bottom-up forcing are temporally variable, and that the presence of macroalgae can strengthen top-down control of epiphytic algae, potentially contributing to eelgrass persistence.