The Ecology and Oceanography of Harmful Algal Blooms

A National Research Agenda

1. Introduction

1.1 The Nature of Harmful Algal
Bloom Phenomena

Among the thousands of species of microscopic algae at the base of the marine food chain are a few dozen which produce potent toxins. These species make their presence known in many ways, ranging from massive "red tides" or blooms of cells that discolor the water, to dilute, inconspicuous concentrations of cells noticed only because of the harm caused by their highly potent toxins. Blooms of non-toxic micro- and macroalgae (seaweeds) also cause harm due either to indirect effects of biomass accumulation (such as anoxia or habitat alteration) or to physical features (such as spines which lodge in fish gill tissue). Impacts of HAB phenomena include mass mortalities of wild and farmed fish and shellfish, human illness and death from contaminated shellfish or fish, death of marine mammals, seabirds, and other animals, and alteration of marine habitats or trophic structure.

The term "red tide" has been used to describe some of these phenomena, since in certain cases, microalgal species increase in abundance until they dominate the planktonic community and discolor the water with their pigments. The term is mislead ing, however, since non-toxic species can also bloom and harmlessly discolor the water or conversely, adverse effects can occur when algal cell concentrations are low and the water is clear. Furthermore, blooms of benthic or planktonic macroalgae can have major ecological impacts such as the displacement of indigenous species, habitat destruction, oxygen depletion, and even alteration of biogeochemical cycles. The causes and effects of macroalgal blooms are thus similar in many ways to those associated with harmful microscopic phytoplankton species. The scientific community now employs the term "harmful algal bloom" (HAB) to describe this diverse array of bloom phenomena.

1.2 HAB Impacts

1.2.1 Public Health and Ecosystem Effects

One major category of public health impact from HABs occurs when toxic phytoplankton are filtered from the water by shellfish such as clams, mussels, oysters, or scallops, which then accumulate the algal toxins to levels that are potentially lethal to humans or other consumers (Shumway, 1990). These poisoning syndromes are named paralytic, diarrhetic, neuro toxic, and amnesic shellfish poisoning (PSP, DSP, NSP, and ASP). Except for ASP, an alarming new syndrome that results in permanent short-term memory loss in victims, all are caused by biotoxins synthesized by a group of marine algae called dinoflagellates. The ASP toxin is produced by diatoms, a group of phytoplankton that until recently was considered free of toxins and generally harmless (Bates et al., 1989). A fifth human illness, ciguatera fish poisoning (CFP), is caused by biotoxins produced by epibenthic dinoflagellates attached to surfaces in many coral reef communities (reviewed in Anderson and Lobel, 1987). Ciguatera toxins are transferred through the food chain from herbivorous reef fishes to larger carnivorous, commer cially valuable finfish. In a similar manner, the viscera of commercially important fish such as herring, mackerel, or sardines are known to accumulate PSP toxins, endangering human health following consumption of whole fish. Whales, porpoises, seabirds and other animals can be victims as well, receiving PSP toxins through the food chain via contaminated zooplankton or fish (Geraci et al., 1989; Anderson and White, 1992). All of these poisoning syndromes occur within the U.S. and its territories.

Another HAB impact occurs when marine fauna are killed by microalgal species that release toxins and other compounds into the water (Box 1.2.1), or that kill without toxins by physically damaging gills or by creating low oxygen conditions as bloom biomass decays. These impacts frequently occur at aquaculture sites where caged fish cannot escape the harmful blooms. Farmed fish mortalities from HABs have increased considerably in recent years, and are now a major concern to fish farmers and their insurance companies. Wild fish, however, may also be affected. The list of finfish, shellfish and wildlife affected by microalgal toxins is long and diverse (Table 1) and accentuates the magnitude and complexity of this one manifes tation of HAB phenomena. It does not, however, adequately document the true scale of that impact.

We are only now beginning to recognize that there can be impacts from toxic blooms in virtually all compartments of the marine food-web due to adverse effects on viability, growth, fecundity, and recruitment. As reviewed by Smayda (1992), toxins can move through ecosystems in a manner analagous to the flow of carbon or energy, and the impacts can thus be far-reaching and significant (Box 3.3.1). In this expanded context, it is evident that our present knowledge base is inad equate even to define the scale and complexity of many HAB phenomena.

Blooms of macroalgae (seaweeds) can also be harmful, especially to seagrass and coral reef ecosystems and the food-webs dependent on those habitats. Nuisance seaweed species replace indigenous macroalgae in the benthos and microscopic phytoplankton in the water column. They thus modify benthic habitats, affect microbial and macrofaunal foodwebs, and alter key biogeochemical features of coastal ecosystems. Because seaweeds are generally benthic organisms and inhabit inshore coastal waters that mark the interface between land and sea, they are often the first primary pro ducers to be impacted by nutrient inputs from land. Indeed, increased nutrient supply seems to be implicated in virtually all harmful seaweed blooms. A dramatic example of the impact of macroalgal blooms was seen in Bermuda, where the green macroalga Cladophora prolifera formed widespread blooms of drifting, filamentous balls that overgrew seagrasses and corals in response to N and P enrich ment from groundwater (LaPointe and O'Connell 1989). This bloom, which many consider to be the most dramatic ecological change in the recent history of Bermuda's waters, led to a dramatic decline in benthic species diversity, including the commer cially-valuable calico clam.

1.2.2 Economic Impacts

The range of the economic impacts from HAB outbreaks and the magnitude of those costs have expanded with increasing public awareness, coastal development, and the growth of mariculture. Shellfish quarantines, wild or farmed fish mortalities, and frightened consumers who avoid seafood (including products which are totally safe) are well-known impacts of major blooms of harmful algae (Ahmed, 1991). Adverse health effects and lost sales of fish and shellfish products are direct costs, but constrained development or investment decisions in coastal aquaculture due to the potential for outbreaks of toxic algae are examples of indirect or hidden costs. Lost marine recreational opportunities are also important indirect costs of harmful algal bloom incidents. Unfortunately, no national estimate of the combined economic costs of HAB phenomena is available. Estimates from isolated, individual events provide some indication of the scale of the problem:

· A single PSP outbreak cost the state of Maine an estimated $7 million in 1980 (Shumway et al., 1988). PSP outbreaks are annual events in Maine, and several have been more severe than the 1980 event.

· An NSP outbreak in 1987-88 closed more than 400 km of North Carolina coastline for shellfishing during the peak harvest ing season, causing economic losses estimated at $25 million (Tester et al., 1991)

· Brown tide outbreaks in 1985 and several succeeding years devastated the New York state bay scallop industry. Economic losses for the fishery were estimated at $2 million per year (Kahn and Rochel, 1988). The brown tide has recurred on Long Island most years since 1985, and continues to have major ecosystem and economic impacts. At this writing, legislation is under consideration to have parts of Long Island declared Disaster Areas as a result of a massive 1995 outbreak.

· In 1987, phytoplankton blooms of the diatom Chaetoceros convolutus were linked to the mortality of 250,000 Atlantic salmon valued at over $500,000 (Rensel et al., 1989). In other years, blooms of the flagellate Heterosigma carterae have caused farmed-fish mortalities in British Columbia and Washington state costing the industry $4-5 million per year (Horner et al., 1991).

· PSP was detected in the rich shellfish beds of Georges Bank in 1989, forcing the closure of those offshore resources. The Georges Bank surf clam fishery alone, closed now for five successive years, has an estimated annual value of $3 million (New England Fisheries Development Association).

· In 1917, the shellfish industry in Alaska produced 5 million pounds of product. Today, except for aquaculture, the state's commercial shellfish industry is virtually non-existent as a direct result of persistent product contamination by PSP (Neve and Reichardt, 1984). The value of the sustainable, but presently unexploited, shellfish resource in Alaska is estimated to be $50 million per year.

· The Gulf coast of Florida experiences frequent red tides, often accompanied by dead fish washed up on beaches, NSP -contaminated shellfish, and human respiratory problems due to toxins aerosolized by the surf. Habas and Gilbert (1974) estimated a loss of $20 million per event, including losses to the tourist industry, hotel/motel suppliers, commercial fisheries, and local governments for the expense of beach cleanup.

· Domoic acid in razor clams and Dungeness crabs in Washington and Oregon in 1991 caused economic losses estimated at $15-20 million (T. Nosho, pers. comm.). Losses included reduced tourist trade, unemployment, reduced or delayed sales, lower prices, and bankruptcy for some commercial processors. Commercial oyster growers experienced declines in both sales and prices during the peak holiday period, although the oysters never contained detectable levels of domoic acid. Some losses continue as razor clam seasons are shortened or closed due to the continued presence of domoic acid in some areas.

· The states of Maine, New Hampshire, Massachusetts, Rhode Island, Connecticut, Florida, California, Oregon, Washington, and Alaska maintain annual shellfish monitoring programs to detect algal toxins in shellfish. The total cost of these programs exceeds $1 million per year.

1.3 Recent Trends

The nature of the HAB problem in the United States has changed considerably over the last two decades (Box 1.3.1). Where formerly a few regions were affected in scattered locations, now virtually every coastal state is threatened, in many cases over large geographic areas and by more than one harmful or toxic microalgal species. Few would argue that the number of toxic blooms, the economic losses from them, the types of resources affected, and the number of toxins and toxic species have all increased dramatically in recent years in the United States and around the world (Anderson, 1989; Smayda, 1990; Hallegraeff, 1993). Disagreement only arises with respect to the reasons for this expansion. Possible explanations include: a) species dispersal through currents, storms, or other natural mechanisms; b) nutrient enrichment of coastal waters by human activities, leading to a selection for, and proliferation of, harmful algae; c) increased aquaculture operations which can enrich surrounding waters and stimulate algal growth; d) introduction of fisheries resources (through aquaculture development) which then reveal the presence of indigenous harmful algae; e) transport and dispersal of exotic HAB species via ship ballast water or shellfish seeding activities; f) long-term climatic trends in temperature, wind speed, or insolation; g) increased scien tific and regulatory scrutiny of coastal waters and fisheries products; and h) improved chemical analytical capabilities that lead to the discovery of new toxins and toxic events.

The trends are equally disturbing for macroalgae. The development of dense canopies of macroalgae in the benthos of shallow water bodies is an increasingly common phenomenon along virtually all of the world's shorelines. Human activities, including deforestation, agriculture, and generation of domestic and industrial wastewaters are increasing the concentrations and fluxes of nitrogen and phosphorus in coastal waters that in turn enhance seaweed productivity leading to high biomass levels (see Box 1.3.2). As with microalgal blooms, these trends are difficult to document statistically due to a lack of long-term datasets, the number of species involved, and the lack of a simple measure of population size or harmful impact that can be tabulated for all outbreaks. Nevertheless, workers in the field are united in their opinion that the problems are worse and the trends disturbing.