Using the hidden isotopic heterogeneity in phyto- and zooplankton to unmask disparity in trophic carbon transfer

Abstract

In this study, we show that natural phototrophic populations can be probed individually for their in situ δ13C signature by linking fluorescence-activated cell sorting and isotope-ratio mass spectrometry (IRMS) using in-line pyrolytic methylation. This novel methodology greatly improved the resolution in discriminating and tracing the differential carbon (C) pathways at the base of the pelagic food web in the cyanobacteria-dominated Lake Loosdrecht (The Netherlands). Our analysis revealed the co-occurrence of phytoplankton taxa differing by 6-10‰ in δ13C. Predominant micro- and mesozooplankton species reflected this difference as the result of preferential grazing and/ or selective digestion. Flow cytometric (FCM) retrieval of phytoplankton δ13C signatures, applied in conjunction with 13C-carbonate labeling, also enabled an assessment of in situ population-specific growth rates. Diatoms and green algae exhibited up to ninefold higher growth rates than those for cyanobacterial species. The coexistence of phytoplankton populations widely differing in δ 13C, standing stock, and turnover time has important implications for the interpretation of C transfer in pelagic food webs. Our approach disclosed a disproportional impact on trophic cascades by numerically minor phototrophs that otherwise would have gone unnoticed. Despite the abundance of cyanobacterial-derived C, the zooplankton largely rely on eukaryotic algae for growth. Rotifers take a central position in passing on this algal C to the cyclopoid copepod populations in the lake. The bosminid-dominated cladoceran population uses both the cyanobacterial- and algal-derived C in approximately equal shares.