Differentiation of morphology and toxicity in harmful algal blooms caused by the raphidophyte alga Heterosigma akashiwo

The purpose of this study was to examine the sequence of changes in the gross morphology and toxicity of the raphidophyte alga Heterosigma akashiwo in the context of blooms of this species in the Strait of Georgia, British Columbia. Field work focused on this alga’s 1989 fish-killing bloom. That bloom was extensive, with discolouration of the water extending from Jervis Inlet through Malaspina Strait into the Strait of Georgia, and south to Cypress Island in Washington State. Excystment events on Spanish Banks in Vancouver harbour preceded population development in the Strait of Georgia during July and August but toxicity was only noted in the last two days of August and through September. Fish kills occurred near Cypress Island, and in Jervis Inlet and the contiguous waters of Agamemnon channel. These locations represented the geographic extremes of the discoloured waters. In Malaspina Strait and Jervis Inlet, information was collected on water column structure, macronutrient concentrations, and the distribution of algae and fish mortalities. Fish mortalities were coincident with the first sighting of waters discoloured with Heterosigma akashiwo in Agamemnon Channel and Jervis Inlet. The alga appeared to be transported to the areas by currents. Algal concentrations were higher at the Malaspina Strait end of a transect into Jervis Inlet and during flood rather than ebb tides. The water column in Malaspina Strait and Jervis Inlet was stratified and both inorganic nitrogen and phosphorus in surfece waters were low enough to limit growth of H. akashiwo. Though this alga can migrate vertically to obtain nutrients at depth, there was no evidence of migration during this toxic event. Termination of the bloom was associated with a weakening of the water column stratification and the reappearance of non-limiting concentrations of nitrogen in the surface waters. Work in culture demonstrated that there was a sequence of reproducible changes in cell size and shape that improved uptake when nutrients were at the concentrations seen in the Strait at the start of the toxic bloom. These changes involved reduction in cell volume by a factor of between 2- and 4-fold and cells changing from rounded, almost football-shaped cells (oblate spheroids), to plate-like (prolate spheroids). Mathematical modeling suggests that the volume changes could improve nutrient uptake by a factor of 21 to 38%. The changes in shape could improve nutrient uptake dynamics by a further 7.5%. Depending on the nutrient history of the population, changes in cell shape could continue beyond the plate-like form with significant portions of the algal population developing surface protuberances when adequate nutrients and energy were available to the population. The elaboration of surface processes could further improve uptake dynamics. A numerical model to describe these shapes was not available so the degree of improvement could not be quantified. As cells reach the end of their life cycle in culture, they revert to the oblate spheroid form and, if no new nutrients are added, will form resting cysts. However, cyst formation can also be triggered earlier in the life cycle by the addition of nutrients. This may benefit the species by ensuring that cells form cysts in shallow waters where spring temperatures are adequate to fecilitate excystment of cells. In addition to changes in shape. Heterosigma akashiwo cells produce a toxic agent which can suppress growth of nutrient competitors and kill predators, or make the algae unpalatable. Production of those toxins begins and declines immediately prior to decline in population numbers. Toxic effects of the alga can be caused to disappear at any time by the addition of nutrients. Similar to the differentiation of cell shape, the level of toxicity expressed by the cells appears to be correlated with the nutrient history of the population. Cells grown in higher nutrient concentrations appear to be more toxic; however, the population need not have high numbers of cells with processes to be toxic. Heterosigma akashiwo would appear to have adaptations which enhance its ability to compete and survive in the nutrient-limited waters of late summer. The adaptions include both changes in gross morphology of the cells and in the production of toxins which reduce the effects of competition and predation. Population growth and formation of concentrations of the alga capable of discolouring the water can be independent of the occurrence of toxicity. Lack of vertical migration and a protracted period of a stable, stratified water column with depleted nutrients appear to be critical to the genesis of toxicity in wild populations.

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