Background Scenario

Harmful Algal Blooms (HABs) have increasingly become a national concern because of their adverse affects on the health of people and marine organisms, as well as the "health" of local and regional economies. The interest in HABs comes from increased public awareness of the negative impacts to marine resources, such as strandings and deaths of marine mammals, birds, and sea turtles. In addition, scientists have determined that there are more toxic algal species, algal toxins, affected fisheries resources, food-web disruption, and economic losses from harmful algal blooms than ever before (Anderson et al. 1993). Interestingly, they are not a new phenomena. There are written references of these toxic species dating back to Biblical times. In fact, dinoflagellates and cyanobacteria have been found in the fossil record for millions of years. Understanding the ecology and oceanography of these species, and how they affect other organisms, including people, continues to be a challenge for researchers. What are the causes and effects of HABs? Where do these toxins typically occur? How can we track the presence of these harmful toxins to prevent health, economic, and marine resource losses? Let’s find out!

What are Harmful Algal Blooms?

Harmful algae blooms (HABs) are microscopic, single-celled plants that live in the sea. HABs is a term used to describe a proliferation, or "bloom," of single-celled marine algae called phytoplankton. Most species of algae or phytoplankton are not harmful and serve as the energy producers at the base of the food web. While there are thousands of algae species in existence, only a few dozen are known to be toxic. These few toxic species produce potent neurotoxins that can be transferred through the food web where they affect and even kill the higher forms of life such as zooplankton, shellfish, fish, birds, marine mammals, and even humans that feed either directly or indirectly on them.

Types of Harmful Algal Blooms

It is a challenge to define harmful algal blooms and to characterize the species that cause them. All HABs were once referred to as "red tides" because of the color imparted by algae suspended in the water, but the description has since become a misnomer because not all HABs are red. Color is imparted through cellular concentrations of pigments like chlorophyll or lower abundance pigments. The HABs that cause red water or "red tide" include the dinoflagellates Alexandrium spp., Karenia brevis,and Noctiluca spp. Some HABs may be brown, yellow, or green, and some may not discolor the water at all. Examples of HABs that are readily associated with brown water discoloration or "brown tide" are the species Aureococcus and Aureoumbra that turn coastal lagoons dark chocolate brown. However, no color is visible in other harmful species, such as the chlorophyll-free dinoflagellate Pfiesteria piscicida and Dinophysis species. Both Pfiesteria and Dinophysis also impart toxicity at very low densities, generally less than 1,000 cells per liter (Burkholder and Glasgow 1997, Smayda 1997).

Causes of Harmful Algal Blooms

The expansion of HABs in the US since 1972 indicate the scale of the problem now compared to 25 years ago has increased significantly. Their presence and persistence represent a significant and expanding threat to human health and marine resources across the nation (Anderson et al. 1993). The numbers and diversity of reported HAB incidents now include almost every U.S. coastal state. Why is this?

Several possibilities should be considered:

• Plants
• Physical relocation
• Pollution
• Temperature and nutrients

Most harmful algal blooms are caused by plants that form the "base" of the food chain. These include both microscopic species of algae, referred to scientifically as phytoplankton. Other HABs are caused by accumulations of nonchlorophyll-containing cells that are similar in form to microscopic algae. A bloom occurs when an alga rapidly increases in numbers to the extent that it dominates the local planktonic or benthic community. Such high abundance can result from explosive growth, caused, for example, by a metabolic response to a particular stimulus such as nutrients or some environmental condition like a change in water temperature, or from the physical concentration of a species in a certain area due to local patterns in water circulation.

Harmful algal blooms also result from physical relocation due to oceanic processes that transport offshore algal populations to inshore regions. For example, the largest blooms observed, those of Trichodesmium in the open ocean, occur far from any coastal inputs (Sellner 1992, 1997). In the Baltic Sea, summer blooms of Nodularia and Aphanizomenon have occurred since late in the last century, likely due to upwelling from meteorological events, or from mixing events induced by North Sea inflows (Sellner 1992, 1997, Kononen and Nommann 1992). The organisms responsible for diarrheic shellfish poisoning, Dinophysis spp., are often swept into coastal bays and river mouths through wind-induced upwelling (Pazos et al. 1995). Blooms of Alexandrium tamarense, responsible for paralytic shellfish poisoning (PSP) in people, are often initiated when cells are transported into the Gulf of Maine from the eastern provinces of Canada, and then further south into Massachusetts Bay (Anderson 1997). Blooms of Karenia brevis, responsible for neurotoxic shellfish poisoning, occur when cells from small, offshore populations in the open Gulf of Mexico move onto the west Florida shelf and into the coastal waters of other states bordering the Gulf of Mexico, and even into North Carolina estuaries (Tester and Steidinger 1997, Dortch et al. 1998). This consistent delivery of many HABs from offshore to inshore regions produces a periodic infusion of potentially dangerous HABs into most areas of the world's coastal oceans, even those that are independent of human actions on shore or coastal watershed activities. As a result, attempts to prevent HAB events are somewhat impractical, because people cannot control general oceanic circulation or even localized coastal currents.

Many people first think that pollution or other human activities cause HABs. On close inspection, however, many of the "new" or expanded HAB problems in the US occurred in waters where pollution is not an obvious factor. The organisms responsible for HABs have been on earth for a long time, so new bloom events may simply reflect better detection methods and more observers rather than new species introductions or dispersal events. Those coastal waters have seen an increase in pollution over the years, but the actual introduction and colonization of the species is the result of natural currents and environmental factors, including a hurricane that occurred immediately prior to a 1972 bloom. It may be that subsequent blooms of this species are enhanced by pollution, but this has not yet been demonstrated. Some believe that man may have contributed to the spreading problem by transporting toxic species in ship ballast water, but this also remains an unproven hypothesis in the United States with respect to HAB species. Another causative factor is that we have dramatically increased aquaculture activities, and these lead to increased monitoring of product quality and safety, revealing indigenous toxic algae that were probably always there.

The linkage to pollution should not be ignored, however, as the increase of nutrient inputs into our coastal waters do stimulate populations of microscopic and macroscopic algae by fertilizing them into bloom proportions. Harmful or toxic species will thus be more abundant and more noticeable. Some scientists even argue that the nutrients that humans supply to coastal waters are delivered in proportions which differ from those that naturally occur, such that we then alter the species composition of the algae by favoring certain groups better adapted to our nutrient supply ratios. One example where nutrient inputs have been linked to harmful blooms is with the ambush predator dinoflagellate Pfiesteria. That organism and many closely related fish-killing species, seem to thrive in polluted waters.

Temperature and nutrients play a role in HAB events, but the exact nature of that role is unclear. In 1997, the west coast of the United States experienced warmer than normal sea-surface temperatures. During the summer and fall of 1997, water temperatures in the eastern Pacific were warmer than usual. In 1998, a transition from El Niño to a La Niña (or cooler than normal waters) occurred along the equator. During the summer of 1998, a large bloom of Pseudo-nitzschia was observed off the coast of California. Toxins produced by these diatoms were responsible for the deaths of various marine mammals. Whether there is a connection between the record El Niño of 1997 and subsequent cooling (La Niña), is not known at this time. That there might be a relationship with these large scale oceanic processes and HAB events is not unreasonable since it is known that warm/cool Pacific Ocean waters have profound effects on weather along the west coast of North America.

Possible Causes of the Increase in Harmful Algal Blooms

The frequency, duration, and intensity of algal blooms are related to a number of biological, chemical, and physical factors, although, many of these complex relationships have not yet been identified. Four possible reasons have been advanced for the increased frequency and expanding geographic occurrence of HABs. First are improved methods of detection and greater monitoring efforts. These increase the probability that a HAB species will be recorded. Second is the introduction of exotic species via ballast water exchange or aquaculture practices (Hallegraeff 1993). A third possibility is that blooms result when grazers fail to control the algal species' growth (Smayda 1990). Fourth, blooms may result from climate changes, as well as human activities, such as increased pollution and nutrient inputs, habitat degradation including dredging, resource harvesting, and the regulation of water flows. All of these reasons are possible explanations for increasing HABs, and one or any combination of them may apply to a particular species.

Human Health and Environmental Effects of Harmful Algal Blooms

The detrimental effects of a harmful algal bloom can range from cell and tissue damage to organism mortality, and can be caused by a number of mechanisms, including toxin production, predation, particle irritation, induced starvation, and localized anoxic conditions. As a result, a bloom may affect many living organisms of the coastal ecosystem, from zooplankton to fish larvae to people.

Only a few HAB species actually produce toxins that are poisonous to people and marine animals. The most well known HAB toxins are generically referred to as:

• ciguatera fish poisoning (CFP)
• neurotoxic shellfish poisoning NSP)
• paralytic shellfish poisoning (PSP)
• diarrheic shellfish poisoning (DSP)
• amnesic shellfish poisoning (ASP)

Pfiesteria piscicida produces two toxins that impact fishes and humans. Cyanobacteria produce similar toxins. Symptoms of exposure to these toxins include gastrointestinal, neurological, cardiovascular, and hepatological symptoms. The terms "fish" and "shellfish" are associated with these illnesses because the toxins concentrate in the fish and shellfish that ingest the harmful algae; people and marine mammals may be poisoned when they consume the affected seafoods.

Economic Consequences of Harmful Algal Blooms

The expansion of harmful algal blooms during the past 25 years is responsible for economic losses approximating $100 million per year (Turgeon et al. 1998). After an outbreak, not only are health issues a major concern, but many industries are also affected. Closures of shellfish beds, lost production in fisheries, severe reductions in local/regional tourism and associated service industries, public illness, medical treatments and advisories result in the loss of millions of dollars per outbreak. Outbreaks typically effect declines in fisheries-related businesses, increased insurance rates, rise in unemployment and bankruptcies, and rise in retail sales for all seafood species. At the same time, public resources are diverted to monitoring programs.

The direct and indirect losses attributed to HAB events are staggering to the local areas where they occur. A single outbreak of paralytic shellfish poisoning in the Northeast was estimated to cost $6 million (Shumway 1988). The 4 to 6-month red tide in North Carolina during 1987-1988 was estimated to have cost the community $25 million (Tester and Fowler 1990). The 1991 outbreak of domoic acid/amnesic shellfish poisoning in Washington had a negative impact on the entire community, from the tourism industry to unaffected fisheries (oysters), with losses estimated between $15 and $20 million. In North Carolina, recent outbreaks of Pfiesteria piscicida and Pfiesteria-like dinoflagellates in 1995 and 1996 have resulted in the deaths of millions of fish, including the commercial menhaden, due to secondary infections and/or toxins (Burkholder and Glasgow 1997). In addition, a recent outbreak of Pfiesteria or Pfiesteria-like organisms in the Chesapeake Bay resulted in a public outcry, an estimated $43 million loss for the seafood industry, and several reported incidents of illness in people (Sieling and Lipton 1998).

Even a nontoxic harmful algal bloom can have devastating effects on a natural community. In South Florida, blooms of macroalgae are overwhelming sections of coral reef ecosystems and seagrass beds (LaPointe 1997). Besides being one of the most productive and diverse marine ecosystems, coral reefs are a vital component of the South Florida economy, attracting thousands of visitors each year. Seagrass beds are important nursery habitat for pink shrimp, spiny lobster, and finfish. Continued overgrowth of algae could eliminate these refuges of biodiversity and lead to severe economic losses for the recreation and tourism industries. In Long Island, brown tide severely impacted the bay scallop industry (Nuzzi and Waters 1989) with the collapse and permanent loss of the $2 million per year industry. In Washington, Heterosigma akashiwo blooms have caused losses of $4 to $5 million per year to harvesters of wild and penned fish (Horner et al. 1997). Finally, in the same region, economic losses due to blooms of Chaetoceros, which mainly affect penned fisheries, are estimated to result in losses of about $500,000 per episode (Rensel 1993a).

Regional HAB Characteristics

Harmful algal blooms occur in all coastal regions of the United States. Although many of the same algae species appear in different regions, bloom conditions are not necessarily similar, nor are they fully understood. While the same species cause the same types of HAB problems in different regions, they may affect different organisms.

The chief HAB in the Northeast, Alexandrium tamarense, is responsible for annual outbreaks of paralytic shellfish poisoning. Alexandrium cells are entrained in two coastal currents in the region. From the Northeast through the Mid-Atlantic region, specifically in lagoonal systems of eastern Long Island, New Jersey, Delaware, and Maryland, brown tide is a recurring HAB problem. Impacts include the loss of submerged aquatic vegetation and the collapse of several shellfisheries, such as the bay scallops of eastern Long Island. The outbreaks occur from late spring to early summer and last from one to four months. Another HAB group common to the Mid-Atlantic region is Pfiesteria piscicida and similar-looking cells known as Pfiesteria-complex organisms. In many environments, P. piscicida and P-complex organisms have co-occurred with high numbers of fish with epidermal lesions, which, over time, may cause death due to secondary infections. This combination of toxins is probably responsible for the recent fish kills in several systems of Maryland's Eastern Shore and in coastal North Carolina.

Southeastern states experience the same problems with Pfiesteria blooms as those in the Mid-Atlantic. In 1995 and 1996, the deaths of thousands, and in a single incident, millions, of fish from the coastal waters of North Carolina were attributed to Pfiesteria or Pfiesteria-like species (Burkholder and Glasgow 1997). Another HAB that has had an impact on southeastern states is Karenia bevis, which produces the toxin responsible for neurotoxic shellfish poisoning (NSP). Blooms are usually seasonal, starting in the late summer to early fall and lasting about three to four months. They appear to derive from offshore Gulf of Mexico populations, to increase over the west Florida shelf, and may later be transported to the South Atlantic Bight via the Loop Current and the Gulf Stream (Tester and Steidinger 1997).

In the Gulf of Mexico, the major HAB problems are brown tides and outbreaks of NSP caused by K. brevis. In the Laguna Madre system of Texas, a dense bloom of the brown tide species Aureoumbra lagunensis persisted for more than seven years after its appearance in 1990 (Buskey et al. 1997). The bloom may have resulted from an unusual weather event during which subfreezing temperatures caused a massive fish kill, which, in turn, provided a pulse of nutrients to the hypersaline lagoonal waters.

On the Pacific Coast, paralytic shellfish poisoning (PSP), amnesic shellfish poisoning (ASP), and finfish mortalities from blooms of the Heterosigma and Chaetoceros species are major HAB problems. Outbreaks of PSP are recurrent, although the bloom dynamics are not well understood. In late May through June 1998, the deaths of more than 50 sea lions, and illnesses in several other sea lions, birds, and sea otters, were attributed to domoic-acid poisoning caused by a bloom of the diatom P. australis off the coast of California near Santa Cruz (Scholin et al. in review). Furthermore, investigating scientists from state, university, and federal labs detected high levels of domoic acid in sardines and anchovies, which are common foods of sea lions (Scholin et al. in review). Lesions of the hippocampus portion of the brain, characteristic of domoic-acid exposure in mammals, were also observed in several of the dead animals.

Off the coast of Washington, little is known about bloom dynamics for any of the HAB species, but parts of the coast have to be closed to bivalve harvesting on a year-round basis. Mass mortalities of penned fish have been recorded in fjords of the region, due to the flagellate Heterosigma and two diatom species of Chaetoceros. In Alaska, recurrent blooms of the PSP-producing Alexandrium species during nearly every month of the year has eliminated the development of any shellfishery, and has caused the deaths of several native people.

Ciguatera fish poisoning is a major problem in tropical regions, and may be the most widespread HAB-generated problem in the world. Caused by benthic dinoflagellates, toxicity results from bioaccumulation of the toxin in the food chain. An example can be seen in the benthic dinoflagellate Gamberdiscus toxicus. Herbivorous fish that eat the macroalgae are eaten by larger fish and so on, until the toxin accumulates in the tissues of top-predator species that are often the primary foods of local island inhabitants.

Karenia brevis - Case Study

Karenia brevis, formerly Gymnodinium breve, is common on the Gulf Coast. K. brevis is the marine dinoflagellate responsible for extensive blooms, commonly called "red tide", that produce potent toxins, called brevetoxins. These toxins cause neurotoxic shellfish poisoning in people and are responsible for killing millions of fish and other marine organisms for centuries. These blooms have been recorded since the Spanish explorations of the late 16th century, and have been reported in 23 of the last 24 years. Recurrent outbreaks have characterized the west coast of Florida and Texas coasts.

Both Texas and Florida have experienced extensive red tides that have had adverse impacts on fishing, the quality of the shoreline, and local economies. A bloom of K. bevis, south of Tampa Bay, killed more than 150 manatees in 1996, and another killed more than 21 million fish along the Texas coast in 1997-1998. Some single events have been estimated to cost $20 million in lost revenues. People can become ill after eating affected shellfish, but more commonly, respiratory distress occurs in compromised individuals, such as older citizens and asthmatics, who have inhaled the toxin while in or near the water.

High cell densities of this toxic dinoflagellate discolor surface waters with a typical red coloration, producing what has commonly been referred to as "red tide." However, prior to actually seeing a "red tide," beach-goers may experience respiratory problems as a result of released toxins that are exuded as an aerosol. The toxic aerosol can affect humans at much lower concentrations than are required for the human eye to actually see discoloration in the water. K. brevis produces brevetoxin, which is lethal to fish and results in massive fish kills that wash up and decompose on local beaches. Fish kills can occur before the water is visibly discolored, at concentrations of ~0.5 million cells per liter. Exposure to brevetoxin can also cause marine mammal mortalities. For example, more than 150 manatees were killed just south of Tampa Bay in 1996.

Within the Gulf of Mexico region, these blooms are considered a natural phenomenon. Bloom initiation, transport, and retention are all strongly affected by the extent of the northward penetration of an offshore, clockwise current known as the Loop Current. Blooms may originate around the fronts caused by the flow of the Loop Current along the outer southwest Florida shelf, approximately 40 to 80 miles offshore (Mote Marine Laboratory 1998 on-line, Tester and Steidinger 1997). The results of these blooms can be both physically and economically devastating to a region. In April 1963, a bloom that occurred from Tampa Bay to Marco Island resulted in the deaths of more than 150 tons of fish, including a 700-pound grouper (Mote Marine Lab 1998 on-line). These incidents and others like them have had severe impacts on several industries, including fisheries (fish and shellfish) and tourism. Blooms have also affected several other wildlife species, including manatees and birds. Besides the 1996 bloom that killed the manatees, a bloom in the Caloosahatchee River area of Florida in 1982 resulted in the deaths of 39 manatees (Landsberg and Steidinger 1998), illustrating the serious impact that these recurrent natural events can have on an endangered species.

There is a strong Florida community awareness and a commitment to reduce the impacts of these nearly annual events on the western coast. Researchers from academic, federal, state, and local organizations, as well as industry and citizen groups, all work to monitor and mitigate the potential effects of harmful algal blooms.

Detection of HABs

Detection of HAB events occur using remote sensing and ground-truthing to increase monitoring efforts and improve methods of detection. Satellite Ocean Color Imagery Maps compiled by NOAA/NESDIS from Coastal Zone Color Scanner and currently SeaWIFS satellites help in the identification of these blooms by detecting chlorophyll levels. This satellite imagery is currently being tested in an experimental phase to provide vital information to alleviate the impact of these financially debilitating and potentially life-threatening events. The use of satellite ocean color imagery, with its ability to repeat coverages, offers the potential to detect and monitor these biological events at appropriate spatial and temporal scales. However, it must be noted that these maps should be interpreted with caution since the use and analyses of the data are still experimental.

Ground-truthing sampling methods via research cruises, have enabled scientists to chart the progression of a bloom. These observations are being used to develop a forecasting ability for the transport of offshore blooms into coastal regions (NOAA Coastal Services Center 1998). With this information, coastal communities will be able to proactively limit the potential impacts of landfall of these toxic populations and the associated fish kills that are deposited on recreational beaches. Using regular cruises for monitoring and sampling, scientists are attempting to understand the environmental, chemical, and physical factors that trigger the accumulation of the toxic species, as well as the factors that induce their toxicity.

Background Scenario adapted from:

Bushaw-Newton, K.L. and Sellner, K.G. 1999 (on-line). Harmful Algal Blooms. In: NOAA's State of the Coast Report. Silver Spring, MD: National Oceanic and Atmospheric Administration. http://state-of-coast.noaa.gov/ bulletins/html/hab_14/hab.html