Contribution of Cell Mortality to the Decline of a Toxic Dinoflagellate Bloom

While numerous laboratory and field studies have greatly increased our understanding of the processes that lead to the initiation of phytoplankton blooms, the mechanisms leading to bloom decline and termination have received less attention. Grazing and sedimentation have been assumed to be the main routes for the loss of phytoplankton biomass, and more recently, viruses, parasites, and programmed cell death (PCD) have been recognized as additional sources of mortality. To better understand the mechanisms contributing to bloom decline, we studied blooms of Alexandrium fundyense at two locations within the Nauset Marsh System (Cape Cod, MA) where this species forms annual blooms. Weekly samples were collected at four depths (1m, 3m, 5m, and 7m) from March to May 2013, covering the periods of bloom initiation, development, and decline. We focused specifically on mortality caused by cell death by measuring reactive oxygen species, caspase activity, and the proportion of dead cells, as well as cell number and size. The number of dead cells with PCD features increased after the peak of the bloom, reaching 10-15% of the total population. We also observed distinct shifts in cell size distributions that are presumed to correspond to life cycle transitions. Over half of the cells were gametes at the peak of the bloom, and they rapidly disappeared as the bloom declined. Our results indicate that A. fundyense cells undergo endogenous cell death, potentially via PCD pathways, during bloom decline. This adds natural cell death as an additional source of cell loss during A. fundyense blooms. In the relatively small and contained system described here, life cycle transitions and parasitism appear to be the biggest contributors to cell loss, with cell death contributing on a similar scale to grazing.