Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea

From 60 to 80 species of phytoplankton have been reported to be harmful; of thcsc, 90% are flagellates, notably dinoflagellates. The effects of turbulence on harmful algal bloom (HAB) taxa, their photoadaptive strategies, growth rate, and nutrient uptake aFlinity (K,) are considered. Flagellates, including HAB taxa, collectively have a lower nutrient uptake affinity than diatoms. Four major adaptations are suggested to have been evolved to offset the ecological disadvantages of their low nutrient affinity: nutrient retrieval migrations; mixotrophic tendencies; allelelochemically enhanced interspecific competition; and allelopathic, antipredation defense mechanisms. Motilitybased behavioral features of flagellates contributing to their blooms include: phototaxis, vertical migration, pattern swimming, and aggregation, which facilitate nutrient retrieval, trace metal detoxification, antipredation, depth-kceping, and turbulence avoidance. Neither a general physiological syndrome nor distinctive physiological profile distinguishes harmful flagellate species from nonharmful taxa. However, HAB tlagcllates exhibit significant ccophysiological differences when compared to diatoms, including greater biophysical vulnerability to turbulence, greater bloom dependence on water-mass stratification, grcatcr nutritional diversity involving mixotrophic tendencies, greater potential use of allelochemical mechanisms in interspecific competition and antipredation defenses, and unique bchaviorial consequences of their motility. Flagellates USC a “swim” strategy; diatoms a “sink” strategy. About 300 (7%) of the estimated 3,400-4,100 phytoplankton species have been reported to produce “red tides,” including diatoms, dinoflagellates, silicoflagellates, prymnesiophytes, and raphidophytes (Sournia 1995). Excluding diatoms decreases this number to -200; moreover, most red tide spccics do not produce harmful blooms. Only 60-80 species (2%) of the 300 taxa are actually harmful or toxic as a result of their biotoxins, physical damage, anoxia, irradiance reduction, nutritional unsuitability, etc. Of these, flagellate species account for 90% and, among flagellates, dinoflagellates stand out as a particularly noxious group. They account for 75% (45-60 taxa) of all harmful algal bloom (HAB) species. The exceptional importance of dinoflagellates is further evident from their pm-eminence among the species, perhaps 10-12, primarily responsible for the current expansion and regional spreading of HAB outbreaks in the sea (Anderson 1989; Hallegraeff 1993; Smayda 1989a, 1990). Harmful algal taxa may be nonmotile or motile; pica-, nano-, or larger sized; photoautotrophic, mixotrophic, or obligate heterotrophs; siliceous or nonsiliceous species, etc., and have diverse modes of inimical action. The considerable physiological and phylogenetic diversity represented in the phytoplankton in general, and among HAB species in particular, prompt a basic question: what cellular processes and environmental mechanisms select for which HAB species, or strains, will bloom, particularly from among those species which co-occur and share overlapping niches? Resolution of this should be a major priority of future research. The equally relevant, better understood question focused upon here is: what common properties of a HAB event must be accommodated ecophysiologically for HAB taxa to bloom? In this analysis, selected ecophysiological attributes of HAB taxa are contrasted with those of diatoms. Diatoms are selected for comparison as the “norm,” because their ecophysiology is better understood than it is for other phylogenetic groups, and with few notable exceptions their blooms do not disrupt food-web processes. Also, the spring bloom-diatom bias and whole-community approach (Smayda 1997) have deflected research away from red tide and HAB events which, until recently, have been generally viewed as periodic, rogue blooms of peripheral scientific interest. Harmful algal blooms, however, provide unique opportunities to evaluate entrenched views based on the spring bloom-diatom template. I consider HAB events to be a scientific Rosetta Stone allowing deeper insights into the underlying principles and processes regulating phytoplankton growth in the sea generally and that of the different phylogenetic groups which have diversified the phytoplanktonic life mode. The selection and treatment of topics in this analysis reflect this view. The need to distinguish between cellular, population, and community growth in bloom dynamics Phytoplankton growth is classically measured as a wholecommunity response, with chlorophyll used as an index of abundance against which rate processes are normalized. Community growth measurements have two presumptions: the community’s taxonomic elements are physiologically equivalent, and chlorophyll-based estimates of community growth rate adequately measure behavior of the dominant taxa. Although these unlikely assumptions have yet to be evaluated, estimates of community growth rate are of considerable biogeochemical value and essential in analyses of mass balance and nutrient flow. However, they provide limited insight into bloom dynamics. In reality, community growth is only one of three different, concurrent growth modes which characterize phytoplankton population dynamics: cellular growth, population growth, and community growth. In analyses of HAB events, community growth is the least significant of the three growth modes, masking