Assimilation of Diazotrophic Nitrogen into Pelagic Food Webs

The fate of diazotrophic nitrogen (N_D) fixed by planktonic cyanobacteria in pelagic food webs remains unresolved, particularly for toxic cyanophytes that are selectively avoided by most herbivorous zooplankton. Current theory suggests that N_D fixed during cyanobacterial blooms can enter planktonic food webs contemporaneously with peak bloom biomass via direct grazing of zooplankton on cyanobacteria or via the uptake of bioavailable N_D (exuded from viable cyanobacterial cells) by palatable phytoplankton or microbial consortia. Alternatively, N_D can enter planktonic food webs post-bloom following the remineralization of bloom detritus. Although the relative contribution of these processes to planktonic nutrient cycles is unknown, we hypothesized that assimilation of bioavailable N_D (e.g., nitrate, ammonium) by palatable phytoplankton and subsequent grazing by zooplankton (either during or after the cyanobacterial bloom) would be the primary pathway by which N_D was incorporated into the planktonic food web. Instead, in situ stable isotope measurements and grazing experiments clearly documented that the assimilation of N_D by zooplankton outpaced assimilation by palatable phytoplankton during a bloom of toxic Nodularia spumigena Mertens. We identified two distinct temporal phases in the trophic transfer of N_D from N. spumigena to the plankton community. The first phase was a highly dynamic transfer of N_D to zooplankton with rates that covaried with bloom biomass while bypassing other phytoplankton taxa; a trophic transfer that we infer was routed through bloom-associated bacteria. The second phase was a slowly accelerating assimilation of the dissolved-N_D pool by phytoplankton that was decoupled from contemporaneous variability in N. spumigena concentrations. These findings provide empirical evidence that N_D can be assimilated and transferred rapidly throughout natural plankton communities and yield insights into the specific processes underlying the propagation of N_D through pelagic food webs.