Trophic lengthening triggered by filamentous, N2-fixing cyanobacteria disrupts pelagic but not benthic food webs in a large estuarine ecosystem.

Abstract

Eutrophication, increased temperatures and stratification can lead to massive, filamentous, N2-fixing cyanobacterial (FNC) blooms in coastal ecosystems with largely unresolved consequences for the mass and energy supply in food webs. Mesozooplankton adapt to not top-down controlled FNC blooms by switching diets from phytoplankton to microzooplankton, resulting in a directly quantifiable increase in its trophic position (TP) from 2.0 to as high as 3.0. If this process in mesozooplankton, we call trophic lengthening, was transferred to higher trophic levels of a food web, a loss of energy could result in massive declines of fish biomass. We used compound-specific nitrogen stable isotope data of amino acids (CSIA) to estimate and compare the nitrogen (N) sources and TPs of cod and flounder from FNC bloom influence areas (central Baltic Sea) and areas without it (western Baltic Sea). We tested if FNC-triggered trophic lengthening in mesozooplankton is carried over to fish. The TP of cod from the western Baltic (4.1 ± 0.5), feeding mainly on decapods, was equal to reference values. Only cod from the central Baltic, mainly feeding on zooplanktivorous pelagics, had a significantly higher TP (4.6 ± 0.4), indicating a strong carry-over effect trophic lengthening from mesozooplankton. In contrast, the TP of molluscivorous flounder, associated with the benthic food web, was unaffected by trophic lengthening and quite similar reference values of 3.2 ± 0.2 in both areas. This suggests that FNC blooms lead to a large loss of energy in zooplanktivorous but not in molluscivorous mesopredators. If FNC blooms continue to trigger the detour of energy at the base of the pelagic food web due to a massive heterotrophic microbial system, the TP of cod will not return to lower TP values and the fish stock not recover. Monitoring the TP of key species can identify fundamental changes in ecosystems and provide information for resource management.