Microscopic Murderer

Most of us know that pollution is a threat to many species on earth. We know that by destroying habitats, humans are pushing many plants and animals toward extinction. But, what people are probably less aware of is that pollution can cause other species to thrive. As global warming causes climate shifts and as more pollutants degrade the land and water for familiar species, other rare species may find conditions favorable and suddenly become prominent. In many cases, these may be species that humans have never seen before. And often, we may wish we had never met them.

Such has been the case with Pfiesteria piscicida. A one-celled creature called a dinoflagellate, Pfiesteria prefers to inhabit warm coastal areas and river mouths, especially along the eastern United States. It has probably existed in these areas for a long time. U.S. Geological Survey scientists have found evidence of Pfiesteria in 3,000-year-old sea floor sediments, and dinoflagellates are thought to be one of the oldest forms of life on earth. Yet, until recently humans never noticed Pfiesteria. That is because, until recently, Pfiesteria probably existed in sparse populations that caused few problems for us.

Lately, however, Pfiesteria seems to be on the rise. Huge, dense populations are becoming more and more common in coastal waters, and in such large numbers, the dinoflagellate becomes a ruthless killer. Large blooms of Pfiesteria emit powerful toxins that weaken and entrap fish that swim into the area. The toxins eventually cause the fish to develop large bleeding sores through which the tiny dinoflagellates attack, feasting on blood and flesh. Often the damages caused by Pfiesteria blooms are astounding. During a 1991 fish kill that was blamed on Pfiesteria on North Carolina's Neuse River, nearly one billion fish died and bulldozers had to be brought in to clear the remains from the river.

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The wounds on these fish were caused by Pfiesteria toxins, which degrade the skin, allowing the organism to feed on the soft tissue and blood cells beneath.
Source: N.C. State University Department of Botany

Of course, such a voracious killer could have a devastating effect on commercially-important fish, but that is just one way that Pfiesteria can cause problems for humans. The toxins that it emits seem to affect human skin much as they affect fish skin, causing bleeding sores on areas that come into contact with Pfiesteria-laden waters. But even staying out of the water is not always enough to protect people from this microorganism. Fisherman and others who have spent time near Pfiesteria blooms report that the toxins seem to get into the air, where once inhaled they affect the nervous system, causing severe headaches, blurred vision, nausea, difficulty breathing, short-term memory loss, and cognitive impairment. People exposed to the toxins have reported losing the ability to do simple arithmetic or find their way home.

For a while, it seemed that deadly Pfiesteria blooms were a threat only to North Carolina waters, but the problem seems to be spreading. In 1997, Pfiesteria was found to be the culprit in a major fish kill in a tributary to the Chesapeake Bay, and fish with lesions typical of Pfiesteria attacks have turned up in Virginia. The organism has even been found in water samples taken from the Gulf of Mexico near Mobile, Alabama. More and more, conditions seem to be favorable along the east coast for Pfiesteria to grow, until, utilizing strength in numbers, the organism is able to attack prey millions of times its size.

Now, researchers are learning that humans are responsible for creating these ideal conditions for Pfiesteria. Pollutants such as animal waste from livestock operations, fertilizers washed from farmlands, and wastewater from mining operations have probably all combined to promote the growth of Pfiesteria in coastal waters. And the results have been devastating.

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Tracking a Fish Killer

A large fish kill is not generally nice to witness. Picture a smooth wide river, glinting in the afternoon sunlight as it slowly flows through coastal forests dotted with tiny towns. Now, picture a small area of this same river suddenly bustling with activity. First a few fish, then more, come to the surface like swimmers gasping for air. Soon, fish can be seen across the entire width of the river. Some end up on the banks, flopping around in the mud as they try to breath. Others float helplessly on their sides in the river. More and more fish appear -- now it seems like there are thousands struggling for life. By the time the sun sets, it is glistening off countless silvery corpses floating in the river, while other fish continue to fight for their lives. During the next day, more fish die, and now the thick smell of their rotting flesh fills the air. Seagulls and other scavengers perch near the water to get first pick at the dead, but there are too many fish for even the birds to eat. Over the course of several days -- sometimes several weeks -- literally millions of fish are killed, turning a peaceful river into the scene of a massacre.

Fish kills like this have long been known to take place occasionally in estuarine environments, places where the fresh water from inland rivers intermixes with ocean saltwater. The common explanation is that at certain times of the year, natural circumstances cause the oxygen levels in the estuary to plummet. Without sufficient oxygen to breath, many of the fish living there die. Generally, though, these fish kills have not been considered that much of a problem. 

But, then, during the late 1980s, a strange thing began to occur in North Carolina. The state's huge estuary system, the second largest in the nation, was becoming the site of more and more fish kills. At first, many locals didn't worry about the dead fish. Many of North Carolina's slow-moving rivers empty into shallow sounds that are separated from the ocean by a long boomerang-shaped island chain know as the Outer Banks. These islands deter the water in the sounds from mixing with the ocean water, and as a result, the area is prone to oxygen deficits.

However, the fish kills in North Carolina were not only becoming more frequent, they were also getting larger. And, there were other differences, too. In nearly half the kills in 1991-1993, the fish would float to the top of the water with holes in them -- large bleeding sores that could not be explained simply by a lack of oxygen. And, when state officials measured the usual indicators of water quality, like pH and dissolved oxygen, they often found nothing out of the ordinary. Sometimes there would be a strange smell in the air near a kill that would burn people's eyes and their throats. This definitely was not just the smell of decaying fish.
 

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Large fish kills caused by Pfiesteria, like this one on the Pamlico River in North Carolina, can affect millions of fish.
Source: N.C. State University Department of Botany

At the same time, many North Carolina fisherman began developing unusual health problems. For one thing, many reported having mysterious sores on their hands and arms that healed very slowly. Others complained that while on the water, they were experiencing headaches and blurred vision. Often these effects didn't subside when they went home. Some were experiencing constant confusion -- difficulty spelling and remembering phone numbers. When one recreational fisherman complained to a doctor, he was given a simple memory test in which he was supposed to repeat a list of 10 items. He found that he could not remember more than three. Later, fishermen in Maryland began complaining of similar symptoms. Though many people realized something was wrong with the water, those who depended on fishing for their livelihood returned day after day, oftentimes becoming progressively more ill.

While more and more people were growing sick and more and more fish were dying, some scientists began to wonder what was happening. Much like detectives looking for a murder suspect, a murder weapon, and a motive, these investigators wanted to know what was killing the fish, how it was killing them, and why it decided to strike when it did. As it turned out, however, the big break in the case wasn't as much the result of good science as it was the result of good luck.

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Finding a Culprit

A little over a hundred miles upstream from North Carolina's estuaries, researchers at North Carolina State University's School of Veterinary Medicine in Raleigh also began experiencing problems with dying fish. Beginning in 1988, tank after tank of the fish that the vet school was raising for experiments would mysteriously perish, and often the dead fish were found riddled with coin-sized wounds. Even pet fish in display aquariums were dying.

When researchers there put some of the aquarium water under a microscope, they found that it was thick with dinoflagellates. At first, though, it was assumed that these organism just thrived in water full of dead fish. No one suspected that these dinoflagellates were the actual killers. That was because fish-killing activity had never been observed before in dinoflagellates.

As members of the protist kingdom, dinoflagellates are technically neither plants nor animals, though in some ways they are both. Some dinoflagellates make their food through photosynthesis like plants, while some eat other organisms for nutrition. Still others are capable of doing both. Though some dinoflagellates had been known to emit powerful toxins, these were generally the plant-like species, and the toxins were released as a way of warding off predators or killing microscopic competitors. Sometimes, these toxins could find their way into seafood, making it unfit to eat, but dinoflagellates had never been know to use toxins to attack and kill large prey.
 

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Pfiesteria piscicida in its most toxic form.
Source: N.C. State University Department of Botany

That is why it was a scientific breakthrough when, in 1991, an N.C. State aquatic botanist named JoAnn Burkholder discovered that a dinoflagellate was not only responsible for killing the fish in the vet school, but that it was also the killer that had been wreaking havoc near the coast. This didn't just mean that Burkholder and her colleagues had discovered a new species of dinoflagellate. They had also discovered a new genus and a new family. The new dinoflagellate was simply unlike anything ever seen before. However, identifying the killer was only the first step in solving this murder mystery. If Pfiesteria was going to be stopped, scientists also needed to figure out how this once unknown dinoflagellate was able to kill fish by the thousands, and why it had chosen now to turn into a killer.

The answer to the latter question came when Burkholder and her colleagues began experimenting with the nutrient levels that Pfiesteria prefers. They found when they increased the levels of nitrogen and phosphorous in the water, the Pfiesteria became much more active. When these nutrients were increased in laboratory aquariums and fish were added, the water would soon become so concentrated with toxin that most types of fish would be killed in a matter of minutes. (In fact the water became so toxic, that several researchers experienced serious health problems as a result of their work.)

Though estuaries in North Carolina normally contain some nitrogen and phosphorous, a variety of sources have likely combined to raise the concentrations of these nutrients in recent years. The increasing use of fertilizers on farms along the banks of North Carolina's major rivers has meant that more of it is washed into estuaries with each rain. Nitrogen and phosphorous are chief components of fertilizer. Along the banks of the Pamlico River, the Texasgulf company operates a huge open-pit phosphate mine that causes elevated phosphorous levels in that river. In July 1992, thousands of fish with lesions were found dead near this mining operation.

However, many people cast most of the blame for elevated nutrient levels on North Carolina's hog farms. During the past twenty years, the state's hog industry has flourished, making North Carolina second only to Iowa in pork production. There are now twice as many hogs raised in North Carolina as there are people living in New York City, and lots of hogs means lots of manure. This manure is extremely rich in nitrogen and phosphorous, yet it is not sent to wastewater treatment plants that remove these nutrients like municipal sewage is. Instead, the hog waste is simply stored in vast lagoons on the farms. With waste from 15 million pigs being stored near North Carolina's rivers, it is easy to imagine that nutrient-laden run-off from these farms might be getting into the state's estuaries. To make matters worse, the waste storage systems at these hog farms have occaisionally failed. For example, in June 1995, a dirt wall collapsed that was holding back an eight-acre lagoon full of hog waste, and, as a result, 25 million gallons of nutrient-rich feces and urine ended up in the New River estuary. Similarly, poultry operations along the tributaries to the Chesapeake Bay have been blamed for allowing Pfiesteria to spread to that area.

No one knows, however, exactly how much these industries are contributing to nutrient pollution in coastal waters. There are other sources of nitrogen and phosphorous, such as golf courses, septic systems, and various industries, that may be making important contributions as well. In addition, removing vegetation and covering land with asphalt and concrete probably exacerbates the problem by decreasing the ground's ability to absorb and cleanse polluted waters. Though it will take further research to uncover exactly how nutrients are entering estuaries, it is clear that humans are altering these ecosyestems and that Pfiesteria welcomes the changes we are making.

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An Amazing Pest

Scientist still do not fully understand how nutrient-rich water causes Pfiesteria to attack fish, but one theory is this: Nutrients in water stimulate the growth of microscopic algae, which is one of Pfiesteria's favorite foods. The dinoflagellates feed on the algae and reproduce until the population is too large for its food source. This causes Pfiesteria to seek other sources of nutrition, which it does by releasing powerful toxins when fish come into the area. The toxins effect the central nervous system of the fish, and they become lethargic and can't swim away. The toxins also disrupt the fishes' ability to maintain their salt balance, which causes their skins to deteriorate, exposing their flesh to the hungry dinoflagellates. (However, some research has shown that certain nutrients stimulate this behavior in Pfiesteria without any algae present.)

When Pfiesteria is in its fish-attacking mode, it looks similar to many other dinoflagellates. It is a bulbus cell with a groove that runs all the way around it. Protruding from this groove are the two tentacle-like flagella that are the defining feature of dinoflagellates. One of these wraps around the cell and the other sticks out into the water. The Pfiesteria uses these flagella to propel itself through the water, swimming in a spiral pattern. When it encounters food, the cell extends a third appendage called a peduncle that looks a little like a trumpet. The Pfiesteria uses the peduncle to attach itself to nearby cells and suck the contents out of them, leaving behind a shriveled membrane.
 

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Some of the many forms of Pfiesteria piscicida.
Source: N.C. State University Department of Botany

But this flagellated form is just one of many different guises for Pfiesteria. For example, if the cells are in the midst of feeding and predators come into the area, some of the cells will turn into much larger amoebas. In the amoeboid phase, the Pfiesteria can engulf and consume most would-be predators, thereby protecting its brothers. Or, if conditions in the water suddenly become unfavorable due to a storm, for example, the Pfiesteria will turn into cysts and drop out of the water column. In the cyst stage, the Pfiesteria are much smaller and protected inside a hard plate-like armor. They sink into bottom sediments where the cysts can survive for very long periods of time, living off of stored food. When conditions again become favorable, the cyst resume their flagellated state and go on the attack again.

In all, scientists have seen Pfiesteria in at least 24 different unique-looking phases, making it an incredibly complicated organism to study. Also complex is the toxins that it emits. Though researchers at Duke University in Durham, North Carolina, have demonstrated that Pfiesteria toxins impair the mental ability of rats, how they act on the nervous system, and what lasting effects they will have on humans that have been exposed to them remains a mystery. In August 1997, scientists isolated and identified one Pfiesteria toxin, but research has been slow. Partly, this is because of the dangers inherent in working with cultures of the deadly dinoflagellate. At least 13 researchers have reported suffering some health effects caused by inhaling the toxins, and now all laboratory work on Pfiesteria must be conducted using Level III Biohazard safety procedures -- the same procedures scientists must use when working with rabies or HIV. Other Pfiesteria research is being conducted to identify the dinoflagellate's effect on commercial fish stocks, and the U.S. Centers for Disease Control and Prevention recently allocated $7 million to study its effects on human health.

But, as we look for ways to identify and mitigate the damage caused by Pfiesteria, we are faced with signs that we may be fighting a losing battle. Other Pfiesteria-like organisms have been implicated in recent fish kills, suggesting that there may be more, similar species that welcome the changes that humans are causing in our environment. And, it is likely that, in the end, the only way we will be able to stem the flow of these new emergent species, is to stem the flow of the pollutants that favor them.

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