Eutrophication reduces seagrass ecosystem stability by decreasing trophic transfer efficiency of energy and fatty acids

Efficient trophic transfer of energy and matter underpins ecosystem functionality, service provision, and stability. The efficiency of energy and matter transfer is jeopardized by various environmental stressors, but their limiting factors might be distinct and require mechanistic elucidation. Addressing this gap, this study examined the transfer efficiency of energy and fatty acids (FAs), and consumer energy budget in a highly representative and widely distributed marine tritrophic food chain under nutrient enrichment using in situ enclosure and lab mesocosm experiments, as well as with a comprehensive global-scale estimation. Our results showed that nutrient enrichment led to a 32.3% decrease in the trophic transfer efficiency of energy, while enhancing the energy loss rate of secondary consumers. Meanwhile, the trophic transfer efficiency of FAs decreased under nutrient enrichment, with the greatest decline in long-chain polyunsaturated fatty acids (PUFAs) reaching 62.1%. Both declines were primarily driven by nutrient-induced shifts in plant–herbivore interaction, mediated by distinct plant traits. Specially, seagrass nutritional quality (starch and total FAs) was the key factor limiting energy transfer efficiency, while chemical defense (total phenols and tannins) predominantly constrained matter transfer efficiency. By scaling these findings through a global estimation, nutrient-enriched seagrass beds may lose approximately 2.0 Tg C of energy and 63.5 × 10⁶ kg of long-chain PUFAs annually through food chain transfer. Such reductions in the trophic transfer efficiency of energy and matter could ultimately compromise ecosystem stability and diminish the quantity and quality of seafood available for human consumption. Therefore, these novel findings advance our understanding of how plant–herbivore interactions mediate the trophic transfer efficiency of energy and matter, and also provide a scientific basis for crucial decisions concerning eutrophication mitigation and the conservation of vital ecosystem services.