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
\nmorphology and toxicity of the raphidophyte alga Heterosigma akashiwo in the context
\nof blooms of this species in the Strait of Georgia, British Columbia. Field work focused
\non this alga’s 1989 fish-killing bloom. That bloom was extensive, with discolouration of
\nthe water extending from Jervis Inlet through Malaspina Strait into the Strait of Georgia,
\nand south to Cypress Island in Washington State. Excystment events on Spanish Banks
\nin Vancouver harbour preceded population development in the Strait of Georgia during
\nJuly and August but toxicity was only noted in the last two days of August and through
\nSeptember. Fish kills occurred near Cypress Island, and in Jervis Inlet and the
\ncontiguous waters of Agamemnon channel. These locations represented the geographic
\nextremes of the discoloured waters.
\nIn Malaspina Strait and Jervis Inlet, information was collected on water column structure, macronutrient concentrations, and the distribution of algae and fish mortalities.
\nFish mortalities were coincident with the first sighting of waters discoloured with
\nHeterosigma akashiwo in Agamemnon Channel and Jervis Inlet. The alga appeared to be
\ntransported to the areas by currents. Algal concentrations were higher at the Malaspina
\nStrait end of a transect into Jervis Inlet and during flood rather than ebb tides. The water
\ncolumn in Malaspina Strait and Jervis Inlet was stratified and both inorganic nitrogen and
\nphosphorus in surfece waters were low enough to limit growth of H. akashiwo. Though
\nthis alga can migrate vertically to obtain nutrients at depth, there was no evidence of
\nmigration during this toxic event. Termination of the bloom was associated with a weakening of the water column stratification and the reappearance of non-limiting
\nconcentrations of nitrogen in the surface waters.
\nWork in culture demonstrated that there was a sequence of reproducible changes
\nin cell size and shape that improved uptake when nutrients were at the concentrations
\nseen in the Strait at the start of the toxic bloom. These changes involved reduction in cell
\nvolume by a factor of between 2- and 4-fold and cells changing from rounded, almost
\nfootball-shaped cells (oblate spheroids), to plate-like (prolate spheroids). Mathematical
\nmodeling suggests that the volume changes could improve nutrient uptake by a factor of
\n21 to 38%. The changes in shape could improve nutrient uptake dynamics by a further
\n7.5%. Depending on the nutrient history of the population, changes in cell shape could
\ncontinue beyond the plate-like form with significant portions of the algal population
\ndeveloping surface protuberances when adequate nutrients and energy were available to
\nthe population. The elaboration of surface processes could further improve uptake
\ndynamics. A numerical model to describe these shapes was not available so the degree of
\nimprovement could not be quantified.
\nAs 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
\nformation can also be triggered earlier in the life cycle by the addition of nutrients. This
\nmay benefit the species by ensuring that cells form cysts in shallow waters where spring
\ntemperatures are adequate to fecilitate excystment of cells.
\nIn addition to changes in shape. Heterosigma akashiwo cells produce a toxic
\nagent which can suppress growth of nutrient competitors and kill predators, or make the
\nalgae 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
\nany time by the addition of nutrients. Similar to the differentiation of cell shape, the level
\nof toxicity expressed by the cells appears to be correlated with the nutrient history of the
\npopulation. Cells grown in higher nutrient concentrations appear to be more toxic;
\nhowever, the population need not have high numbers of cells with processes to be toxic.
\nHeterosigma akashiwo would appear to have adaptations which enhance its
\nability to compete and survive in the nutrient-limited waters of late summer. The
\nadaptions include both changes in gross morphology of the cells and in the production of
\ntoxins which reduce the effects of competition and predation. Population growth and
\nformation of concentrations of the alga capable of discolouring the water can be
\nindependent of the occurrence of toxicity. Lack of vertical migration and a protracted
\nperiod 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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