Complexity in the eutrophication-harmful algal bloom relationship, with comment on the importance of grazing

This article seeks to guide the conceptual development and field application of the eutrophication-HAB hypothesis. After considering the evidence for this hypothesis, the importance of exogenous nutrients as a chemical habitat conditioner and the family of nutrient regulated effects that occur are discussed. The various definitions of eutrophication are applied; the conceptual ambiguity over how to perceive eutrophication, and the need to view eutrophication as a process and not as an ecological state are considered. The habitat irradiance-nutrient-flushing gradient regulates the bloom potential in response to exogenous nutrients. There is an apparent species-specific paradox within the eutrophication-HAB hypothesis related to the phycotoxin synthesis-nutrient relationship. Two nutrient-toxin relationships occur: toxin biosynthesis during nutrient sufficiency, and biosynthesis that requires a nutrient limitation. HAB events can be just as much nutrient depletion events as nutrient stimulated events, and whether the former develops depends upon the specific cellular toxicity-nutrient relationship of the bloom species. The importance of grazing in bloom regulation is highlighted. HABs and red tides generally should be viewed as blooms that are regulated by coupled nutrient-grazer processes - nutrient stimulation alone is inadequate, even when exogenous nutrients are not a factor. In assessing the eutrophication-HAB relationship, the collective grazing behavior of the micro-zooplankton, herbivorous copepods, filter feeding benthos, benthic larvae and, when present, omnivorous nekton must be considered. The importance of grazing in the bloom behavior of HAB species is illustrated using field and experimental data during a 5-month brown tide in Narragansett Bay. A cascade in grazing pressure regulated this bloom, with the initial collapse and then restoration of grazing pressure progressing through 7 stages of collective grazing pressure by micro-zooplankton, herbivorous copepods, benthic larvae, benthic filter feeders, and lytic virus infection. (C) 2008 Elsevier B.V. All rights reserved.