COS 298-1 - The coupling of green and brown food webs by mammalian consumers regulates trophic structure and nutrient cycling in terrestrial ecosystems

Abstract: Food web ecology has revolutionized our understanding of ecological processes, but the drivers of food web structure and its consequences for ecosystem functions are notoriously enigmatic. In terrestrial ecosystems, above- and belowground systems were historically compartmentalized into “green” and “brown” food webs, but the coupling of these systems by animal consumers is increasingly recognized. Indeed, increasing evidence suggests microbial decomposers in brown webs are key to regulating energy flow in many ecosystems by transforming recalcitrant plant matter (e.g., cellulose) into essential biomolecules like amino and fatty acids. Here, we use stable isotope analysis (δ¹³C, δ¹⁵N) of individual amino acids to trace the flow of essential biomolecules through food webs and jointly measure food web coupling, trophic structure, and nutrient cycling by small mammals in New Mexico and Alaska. First, we tested the hypothesis that brown energy fluxes to aboveground consumers increase terrestrial food chain length via cryptic trophic transfers during microbial decomposition. We show that the average small mammal consumer in a montane forest of New Mexico acquires nearly 70% of their essential amino acids (69.0% ± 7.6) from brown food webs, leading to significant increases in trophic position across species and functional groups. Second, we explore the effects of climate-mediated permafrost decay on food web coupling and nutrient cycling by small mammals in Alaska, and we show that increased decomposition of permafrost has led to a state-change in Boreal food webs such that previously green food webs are now entirely fueled by brown energy. Further, we show that the amount of brown carbon stored in aboveground trophic compartments has more than doubled over 30 years, a flux of >500 kg C km^-2. In both systems, we show that fungi are the primary conduit of brown energy to aboveground consumers, providing approximately half the amino acid budget for small mammals on average (44.3% ± 12.0 in NM, 56.8% ± 26.7). These findings illustrate the critical role of mammalian consumers in mediating energy flow across ecosystem boundaries, and highlight the tightly coupled nature of green and brown food webs in terrestrial ecosystems. Lastly, our data show that microbial processes mediate the flow of energy through terrestrial food webs and underscores the importance of bottom-up processes in regulating food web structure.