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Volume 15, Number 4 • July-August 1997
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Toxic Algae

Dinoflagellates, Protists and Pfiesteria

Harmful Algal Blooms on the Move

Also visit:

Alien in Our Midst?
(Marine Notes March 1993)

Pfiesteria and Pfiesteria-like Organisms

Fish Health in the Chesapeake Bay

SPOTLIGHT ON RESEARCH:

In Harm's Way?
The Threat of Toxic Algae

[fish with sores (JoAnn Burkholder)]


By Jack Greer

Flying a small plane some 500 feet above the Chesapeake Bay, researcher Larry Harding can easily observe changes in color - from green, to brown to mahogany and even red. But Harding, a scientist at the University of Maryland Center for Environmental Science (UMCES), and his colleagues do not depend on the eye. They have on board highly sophisticated computerized "ocean color" instruments, that, when properly interpreted, can "read" chlorophyll levels and signal the location and density of phytoplankton blooms throughout the Bay.


Red tides are not necessarily toxic, although at times even harmless species can cause fish kills by depleting the water of oxygen.


In spring, much of that phytoplankton is comprised of diatoms - these minute plants use silica to form skeletons that, under the microscope, look like delicate geodesic domes or Roman amphitheaters. By mid-summer diatoms have largely given way to other forms of phytoplankton, including blue-green algae and dinoflagellates.

While diatoms float through Bay waters, dinoflagellates are generally more active. Using their flagella - slender whip-like tails - they propel themselves about, acting very much like animals, though half contain chloroplasts and perform photosynthesis like other algae. Actually neither plant nor animal but "protists," these tiny organisms cause blooms that we call "red tides."

Dinoflagellates, along with diatoms and many other single-celled organisms, form part of the Chesapeake's normal cohort of microscopic life. In other parts of the world, however, dinoflagellates have for years attracted attention because a few - less than two percent of the known species - can contain very powerful biotoxins.

When Tides Turn Red

For many years people living in South Florida have seen dinoflagellate blooms come and go. They call them red tides because the dinoflagellates in question - such as Gymnodinium breve - have a reddish color due to photosynthetic pigments and appear to turn water the color of blood.

Red tides are not necessarily toxic, although at times even harmless species can cause fish kills by depleting the water of oxygen. Toxic forms have more dramatic effects - extensive fish kills in some cases, or even impacts on human health. Blooms of Gymnodinium breve, for example, can cause eye and throat irritation of shore-dwellers, when surf and wind combine to atomize the toxin and waft a noxious mist inland. Such was the case in coastal North Carolina in 1987, when an errant spiral off the Gulf Stream sent a bloom of toxic dinoflagellates toward Atlantic beaches.

But at least since 1991, North Carolina - and now Maryland - have been preoccupied with another dinoflagellate, not a typical red tide organism, but one with a remarkable ability to use its toxin to stun fish and feed on them. This dinoflagellate, Pfiesteria piscicida, is the only dinoflagellate known to use a toxin in precisely this way. "Usually dinoflagellates produce toxins internally, what we call endotoxins," says Sea Grant Extension specialist Dan Terlizzi. "These can be released when the cells die and break up," he says, "but Pfiesteria employs an exotoxin, meaning that it emits the toxin as part of a direct attack on its prey."

Although Pfiesteria shares characteristics with many other dinoflagellates, it does not cause visible "red tides," and its attack strategy and multiple life stages tend to set it apart. According to research by JoAnn Burkholder and others at North Carolina State University, Pfiesteria assumes more than twenty different forms during its lifetime, including a difficult-to-detect cyst stage; an amoeboid stage; and a toxic vegetative stage, in which, propelled by its flagella, it can kill fish.

In North Carolina, Pfiesteria was implicated in the fish kill of some one million menhaden, and caused the closing of ten miles of river to fishing and swimming. Estimates are that fish kills with possible links to Pfiesteria have claimed a billion fish in that state so far.



Since last fall, when fish began showing lesions in the Pocomoke dinoflagellates, especially Pfiesteria, came under suspicion.

Drawing on both Biblical language and the image of red tides, writer Rodney Barker has written a book about Pfiesteria entitled, And the Waters Turned to Blood. Early press about the book cast Pfiesteria as something of a plague, as "deadly as the Ebola virus" - exaggerated claims that caused widespread concern and seemed to have misled some into thinking that Pfiesteria is an infectious disease organism, like a bacterium or a virus.

Clearly, toxic dinoflagellates may have human health effects. In some areas outside the Bay - in the Pacific Northwest and Alaska, for example, and in Maine - dinoflagellates have caused diseases in humans such as paralytic shellfish poisoning. In tropical areas, ciguatera toxin from dinoflagellates accumulates in the flesh of fish and shellfish and can cause food poisoning. In North Carolina, researchers working with Pfiesteria in the laboratory reported neurological and other health problems, and watermen in Maryland's Pocomoke River area have reported fatigue, respiratory problems, weight loss and other ailments after working in waters where they caught fish with lesions.

Whether the ailments reported in the Pocomoke are related to Pfiesteria, Pfiesteria-like organisms, or to some other cause remains uncertain, but clearly something unusual is going on in that quiet Eastern Shore river.

Trouble on the Pocomoke

On August 6, waterman Eddie Johnson, along with Sheila Tanata, a fisheries biology student at the University of Maryland Eastern Shore, began to see large numbers of dead fish in the Pocomoke River. Soon estimates began to come in of thousands of dead menhaden, croaker, and other species, many - about a third, according to some reports - with lesions.

Once again Pfiesteria and its relatives became prime suspects.

Since last fall, when fish began showing lesions in the Pocomoke, dinoflagellates, especially Pfiesteria, had come under suspicion. But there are many other reasons why fish suffer from lesions, and so state agencies have struggled to understand exactly what is happening in this low-lying tributary that runs along the Maryland-Virginia line.

With uncertainty and concern mounting as the summer progressed, Governor Parris Glendening called, just days before the fish kill, for an interagency team to meet near the Pocomoke to share information about fish lesions and their possible cause.

Donald Boesch, President of UMCES, was appointed to head a technical advisory committee that included experts in algae and dinoflagellates, water quality and fish diseases. JoAnn Burkholder, an authority on Pfiesteria from North Carolina State University and a member of the committee, attended the Pocomoke summit, along with representatives from the Maryland Department of Natural Resources, the Maryland Department of the Environment, the Maryland Department of Health and Mental Hygiene, the Maryland Department of Agriculture, The Academy of Natural Sciences, and the University System of Maryland. Other scientists from Maryland, Virginia, Delaware, and Florida joined the group.

According to Boesch, determining the nature of the problem will require careful monitoring coupled with experimental studies. Only by sampling over time, he says, will we be able to determine whether this is a "short-term" or a "long-term" problem.

The state is taking a close look at a number of possible causes of lesions and fish kills, including harmful chemicals, infections by bacteria and fungi, and other harmful microorganisms, including Pfiesteria piscicida. There is some thought that changes in runoff and water chemistry (including salinity) could play a role, especially since 1996 was one of the wettest years on record, followed by a very dry summer.

The advisory committee discussed the importance of runoff, and though they determined that there is "no demonstrable cause and effect linkage," nonpoint inputs - such as nutrients and pesticides - should, they said, be a primary focus of study.

Prognosis for the Bay

Is the appearance of Pfiesteria the first sign that the Bay's luck has run out?

"Every year in Chesapeake Bay and its rivers, diatoms and dinoflagellates produce seasonal blooms," says Harold Marshall of Old Dominion University, "and in most cases they are harmless." But, he adds, "there is some evidence that concentrations of potential toxin producers now living in the Bay are increasing." Marshall, who has tracked phytoplankton in the Bay for the past three decades, says that this increase may be due to human impacts such as increased nutrients, or it may be due to changing environmental factors. Or both.

[diatom]

Dinoflagellates and diatoms, like the one pictured above,
produce seasonal blooms in the Chesapeake Bay
every year, most of them harmless.



These changes, says Marshall, "may also enhance the development of newly observed and dangerous species," which, he says, have "the potential for expanding their distribution within the estuary."

For the past twelve years, Marshall has cooperated with others in the northern Bay, including Kevin Sellner and Richard Lacouture of the Academy of Natural Sciences Estuarine Research Center, to track phytoplankton blooms - their evaluation report is due out this fall.



"There is some evidence that concentrations of potentioal toxin producers now living in the Bay are increasing."


Marshall has identified nine dinoflagellates, as well as three diatoms, which are toxin producers in other parts of the world. Add another two dinoflagellates and one diatom from previous reports, and that adds up to fifteen known species that could produce toxic blooms in the Bay.

What is puzzling - and fortunate - is that so far none have apparently done so.

Says Marshall, "The enigma regarding many phytoplankton species is that not all of the potential toxin producers will produce toxins, or blooms in their respective habitats."

Why not? "Maybe," he says, "these species have not been exposed to the specific environmental conditions that would initiate their toxin production." Or, he suggests, perhaps these dinoflagellate populations found in the Bay represent non- or less virulent strains of toxin producing species.

Whatever the reason, in the Chesapeake Bay we have been extremely lucky. Despite the Bay's battle against nutrients and contaminants - made more difficult by continuing growth and development in the watershed - large dinoflagellate blooms in the estuary have remained non-toxic.

Marshall cites an example. During mid-summer to early fall in 1992, a bloom of the dinoflagellate Cochlodinium heterolobatum Silva spread from the mouth of the York River into the lower Chesapeake Bay and out the Bay's mouth. Nearshore currents carried the bloom toward North Carolina. At one point, Marshall reports, the bloom spread over 83 square miles of the central and western Chesapeake Bay.

Previously, he says, blooms of this species were generally localized in the York River. Since 1992, this dinoflagellate has apparently expanded its range, and has become an annual bloom producer in several rivers of the Chesapeake, according to Marshall.

This same species has caused fish kills in culturing grounds in Japan and reduced calcium uptake and elevated oyster larvae mortality in lab studies in New York. Karen Steidinger, an expert on dinoflagellate blooms with the Florida Department of Environmental Protection, lists this species as a toxin producer, though it has not caused large fish kills in the Bay.

Other examples abound. Kevin Sellner and Mark Luckenbach, a scientist at the Virginia Institute of Marine Science, have noted that Prorocentrum minimum, a common Bay dinoflagellate, induces high mortalities in juvenile oysters in lab studies. Fortunately there has been no observation of any impact in the Bay.

Further, according to Gail Mackiernan, who was studying dinoflagellates at the time in Virginia, in 1967 a dense bloom of Gonyaulax monilata covered much of the southern Bay from just north of Mobjack Bay nearly to the mouth of the Bay. That dinoflagellate is a known toxin producer and is responsible for fish kills in both Florida and Texas. "The bloom persisted for more than a month," says Mackiernan, Assistant Director for Research at Maryland Sea Grant, "but in the Bay it had no apparent effect on fish."



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