Herbivore community determines the magnitude and mechanism of nutrient effects on subtropical and tropical seagrasses

1. Numerous studies have examined the combined effects of nutrients (bottom-up control) and consumers (top-down control) on ecosystem structure and functioning. While it is recognized that both can have important effects, there remains a limited understanding of how their relative importance shifts across large spatial scales where consumer functional types can vary. 2. Using seagrasses as a model ecosystem, we explore the effects of ambient variation in herbivore functional composition on the relative importance of bottom-up and top-down forcings. Distributed experiments were conducted across four Western Atlantic sites that encompassed a gradient in consumer composition. Herbivores at two subtropical sites were predominantly comprised of small crustacean invertebrates (mesograzers that consume epiphytic algae), while herbivores at two tropical sites were dominated by large macrograzers (sea urchins and herbivorous fishes that directly consume seagrass biomass). 3. To test the relative importance of bottom-up and top-down factors at each site, we manipulated nutrient supply, mesograzer abundance, and the presence of macrograzers (mainly herbivorous fishes) in a fully factorial design over a 14-week growing season. Seagrass above-ground biomass, shoot density, canopy cover, leaf productivity and epiphyte mass were measured as indicators of habitat structure and productivity. 4. Overall, nutrient addition elicited a strong response across sites, causing widespread loss of seagrass biomass and shoot density. However, the mechanisms driving these declines strongly varied as a function of resident herbivore identity. Seagrass loss at tropical sites was attributable to macrograzers, which increased their direct consumption of fertilized, nutrient-rich seagrass. Conversely, at the subtropical sites, nutrient loading caused seagrass declines associated with the proliferation of epiphytic algae, but only in locations where mesograzer abundance was low. 5. Synthesis. Our results confirm that nutrient enrichment generally has negative effects on seagrasses, but that the underlying mechanisms vary and may depend upon herbivore presence and functional identity. Along a subtropical to tropical gradient, the adverse effects of nutrient loading may switch from competitive algal overgrowth to a stimulation of seagrass consumption. Thus, in the tropics, top-down and bottom-up factors can act in combination, and in the same direction, to contribute to habitat loss.