CO2 and nutrient-driven changes across multiple levels of organization in Zostera noltii ecosystems

Increasing evidence emphasizes that the effects of human impacts on ecosystems must be investigated using designs that incorporate the responses across levels of biological organization as well as the effects of multiple stressors. Here we implemented a mesocosm experiment to investigate how the individual and interactive effects of CO2 enrichment and eutrophication scale-up from changes in primary producers at the individual (biochemistry) or population level (production, reproduction, and/or abundance) to higher levels of community (macroalgae abundance, herbivory, and global metabolism), and ecosystem organization (detritus release and carbon sink capacity). The responses of Zostera noltii seagrass meadows growing in lowand high-nutrient field conditions were compared. In both meadows, the expected CO2 benefits on Z. noltii leaf production were suppressed by epiphyte overgrowth, with no direct CO2 effect on plant biochemistry or population-level traits. Multi-level meadow response to nutrients was faster and stronger than to CO2. Nutrient enrichment promoted the nutritional quality of Z. noltii (high N, low C :N and phenolics), the growth of epiphytic pennate diatoms and purple bacteria, and shoot mortality. In the low-nutrient meadow, individual effects of CO2 and nutrients separately resulted in reduced carbon storage in the sediment, probably due to enhanced microbial degradation of more labile organic matter. These changes, however, had no effect on herbivory or on community metabolism. Interestingly, individual effects of CO2 or nutrient addition on epiphytes, shoot mortality, and carbon storage were attenuated when nutrients and CO2 acted simultaneously. This suggests CO2-induced benefits on eutrophic meadows. In the highnutrient meadow, a striking shoot decline caused by amphipod overgrazing masked the response to CO2 and nutrient additions. Our results reveal that under future scenarios of CO2, the responses of seagrass ecosystems will be complex and context-dependent, being mediated by epiphyte overgrowth rather than by direct effects on plant biochemistry. Overall, we found that the responses of seagrass meadows to individual and interactive effects of CO2 and nutrient enrichment varied depending on interactions among species and connections between organization levels.