Cell death in individual freshwater phytoplankton species: relationships with population dynamics and environmental factors

Abstract

ABSTRACT Understanding and predicting changes in phytoplankton populations requires knowledge of losses due not only to sedimentation and grazing, but also to intrinsic processes (here, collectively termed ‘cell death’). Cell death is poorly understood, especially in freshwater phytoplankton, but experiments in culture often suggest involvement of abiotic factors (e.g. temperature, light, nutrients). The occurrence of cell death was examined in a simple, natural environment: a small, well-mixed, temperate, urban pond during a period of phytoplankton growth, from mid-July to mid-November. Abundances of 18 phytoplankton taxa were measured weekly and fluorescence microscopy and staining was used to detect dead cells (using SYTOX which measures loss of membrane integrity) and cells undergoing cell death (using Annexin-V, which measures lipid inversions of membranes, an early signal of cell death). Dead and dying cells occurred in most phytoplankton taxa, but incidence and timing varied considerably, e.g. species like the chlorophyte Ankistrodesmus spiralis showed 20–30% of cells staining with SYTOX and Annexin in late autumn when the population was decreasing, while the dinoflagellate Peridinium sp. showed staining of up to 50% of cells with STYOX throughout the period, and the cyanobacterium Microcystis aeruginosa occasionally showed staining of 100% of cells with SYTOX. Overall, there was some association between cell death staining and growth phase with 10–15% of the total community showing SYTOX and Annexin staining in late autumn, when most populations were declining. Cell death could not be correlated with thresholds or rapid changes in abiotic conditions (e.g. temperature, irradiance) or with indicators of nutrient limitation (e.g. N:P ratios). While abiotic factors have been clearly implicated in cell death within unialgal culture experiments, in natural freshwater ecosystems interactions between biotic factors, such as pathogens or allelopathy, may play greater roles in losses related to cell death and be distinct for different taxa.