Properties and Behavior of Sexual Life Stages Underlying Dinoflagellate HAB Events of Cyst-Producing Species That Disrupt Fisheries and Aquaculture

Abstract

Harmful algal blooms (HAB) are natural environmental occurrences that can disrupt ecosystem function that supports fisheries and aquaculture, as well as rendering harvested seafood, especially shellfish, unsafe for consumption by humans or wildlife species. Many dinoflagellates that cause HAB have a life cycle with a sexually produced resting stage called the resting cyst. The resting cyst enables the species to persist in an area where conditions for growth vary seasonally. These species often are found as vegetative stages only during a short period of the year. Most of the time is spent dormant or quiescent as thick-walled resting cysts with very low metabolic activity. By summarizing findings from an iterative series of research projects investigating different parts of the sexual life cycle, a more complete picture of the role of the sexual stages emerges, illuminating the consequences of life cycle within the environmental context. Gametes, the sexual stages, are formed at the end of the growing season in response to environmental signals which remain largely unknown. Gametes have lower cell-specific density and different swimming behavior compared to vegetative cells. Specifically, vegetative cells perform daily vertical migrations; whereas, gametes accumulate in patterns influenced by lower cell-specific density, changed swimming behavior, and attraction to each other. The patterns and patches of accumulated gametes (sexually induced cells) aggregate into larger and larger patterns. Together with large-scale hydrographic water movements, such as upwelling, water stratification, and fronts, cells originating from a low vegetative cell density background distribution assemble and become concentrated within a constricted space, thus forming a dense “bloom.” This process is distinctly different from the paradigm of blooms resulting from simple, vegetative cell divisions. Undisturbed blooms of cyst-producing dinoflagellate gametes end with gamete fusion into diploid zygotes that transform into resting cysts. The resting cysts sink according to shape and cell-specific density into the silt fraction of the sediment. Cyst preservation depends upon the oxygenation level of the sediment and the presence of fauna. Hypoxic/anoxic conditions lower cyst mortality from benthic grazers. The reestablishment of motile, vegetative cells occurs under seasonally favorable conditions, and successful population growth depends upon environmental conditions, such as weather and nutrient availability. Factors that increase HAB risks of resting cyst-producing dinoflagellates are eutrophication leading to high cell numbers and high cyst preservation in hypoxic benthic zones. Hydrographic factors causing increased cell accumulation also are important, and intensified water stratification can amplify encystment success. These insights underscore mechanisms by which climate change is affecting HAB ecology and subsequent effects upon marine and coastal fisheries and aquaculture.