Strategies of amino acid supply in mesozooplankton during cyanobacteria blooms: A stable nitrogen isotope approach

Abstract

Knowledge of how zooplankton can utilize cyanobacteria to sustain their nitrogen (N) demand for essential compounds like amino acids (AAs) is a key to predicting responses of higher trophic levels in terms of production and food web structure to future enhanced water column stratification. We explored the natural abundances of bulk N and AA-specific nitrogen isotopes (δ15N) in particulate organic matter and mesozooplankton size-fraction samples from three vertically separated water bodies in the central Baltic Sea during two summertime cyanobacteria blooms. The combination of plankton community and isotope data together with environmental variables helped to identify a mechanism of diazotrophic AA supply (synthesized during N2 fixation) for mesozooplankton, that largely depended on the sea surface temperature which regulated the access to the diazotrophic N-based food web in the surface water (SW). We found that in the warmer summer, thermophilic cladocerans (e.g., Bosmina spp.) benefited most from diazotrophic AAs in the SW (19.8°C), while only in the colder summer, temperate copepods (e.g., Temora longicornis) ascended from the subjacent winter water into the SW (16.2°C) and incorporated diazotrophic AAs. Trophic position estimates based on the phenylalanine and glutamic acid δ15N signatures revealed that the diazotrophic AA supply into mesozooplankton was mainly indirect via feeding on mixo- and heterotrophic diets. Significantly enriched δ15N signatures in phenylalanine in the deep mesozooplankton (mainly copepods of Pseudo- and Paracalanus spp.) from the bottom water (BW) that was a region of the suboxic zone point to a reliance on a local food web. Mesozooplankton in the BW was feeding on diets of heterotrophic origin and probably profited from the heterotrophic re-synthesis of AAs originating from sinking organic matter, as well as from the indirect incorporation of de novo synthesized AAs that most likely originated from chemoautotrophic bacteria or archaea communities in the suboxic zone. Our findings suggest that indirect feeding on diazotrophs and chemoautotrophs will be principal ways of amino acid supply for zooplankton in future enhanced stratified aquatic systems. Only a relatively small increase in temperature may restrict temperate key species from diazotrophic N-based food webs in the mixed layer.