Does ancient permafrost-derived organic carbon affect lake zooplankton growth? An experimental study on Daphnia magna

The popular paradigm in trophic dynamic theory is that contemporary autochthonous organic matter (e.g., phytoplankton) sustains consumer growth, whereas aged allochthonous organic matter is conceptually considered recalcitrant resources that may only be used to support consumer respiration but suppress consumer growth. This resource-age paradigm has been challenged by a growing body of recent evidence that ancient (radiocarbon depleted) organic carbon (OC) released from glaciers and permafrost can be incorporated by consumers in aquatic systems. However, little information is available regarding the food quality of ancient terrestrial OC and how it impacts the growth of consumers in lakes. Here, ancient dissolved organic carbon (DOC) was extracted from frozen soils in an alpine lake catchment. The contents of polyunsaturated fatty acids (PUFAs) in soil DOC increased significantly after bioconversion by heterotrophic bacteria. The utilization of soil DOC by heterotrophic bacteria also increased the total phosphorus concentration in the systems. Gammaproteobacteria and Betaproteobacteria showed a strong negative correlation with the percentage contents of fluorescent components, including humic-like and tyrosine-like components. Daphnia magna were fed Auxenochlorella vulgaris and ancient DOC plus heterotrophic bacteria. The contents of PUFAs and the growth of zooplankton were influenced by the pre-conversion time of ancient DOC by bacteria. When ancient DOC was pre-converted by bacteria for 27 days, D. magna fed on the mixed diets showed the highest body length (3.40 mm) and intrinsic rate of increase in population (0.49 d⁻¹). Our findings provide direct evidence that ancient terrestrial OC can be an important subsidy for lake secondary production, which have important implications for food webs in high-altitude and polar lakes.