The majority of the information in this document results from work conducted in JoAnn Burkholder's laboratory. Additionally, federal, state and academic scientists reviewed and contributed to the information in the Glossary.
Please contact one of the following individuals before any formal publication or reference: Judy Kleindinst jkleindinst whoi. Scientists now prefer the term "harmful algal bloom" or HAB over "red tide" because the water is not always discolored when blooms cause damage, and conversely, the situation is often harmless even when the water is quite red.
This question correctly notes that there has been an increase in the occurrence of toxic and harmful algae blooms over the last several decades. The evidence comes from increasingly frequent scenes of dead and rotting fish on beaches; shellfish harvesting quarantines; dead whales, manatees and other marine animals; and a number of other highly visible outcomes.
The latest species to join this list of organisms causing HABs is Pfiesteria piscicida , unknown to science seven years ago. Since its discovery in a North Carolina estuary, Pfiesteria and closely related organisms have been reported in Florida, Virginia and Maryland estuaries, and they no doubt occur in many other adjacent states.
Pfiesteria causes harm to humans and to a variety of marine animals, especially fish. Strictly speaking, Pfiesteria is not an alga but belongs to a group of single-celled organisms called dinoflagellates. It has been included under the umbrella term HAB because it shares many ecological, toxicological and genetic characteristics with other HAB species.
The mature stage, shown here, resembles an amoeba. Scientists are in agreement that there are more harmful algal species, more toxins, more fisheries resources impacted, more areas affected and higher economic losses than ever before. The general public and politicians are quick to blame pollution for these increases, as the HAB species are plants that thrive on the nutrients contained in sewage and other pollutants.
In reality, however, only some of the HAB outbreaks can be linked to pollution. The best linkage is probably with Pfiesteria , which is most frequently encountered in polluted waters.
In North Carolina, these are areas downstream from hog farming operations, and in Maryland, downstream from large chicken farms. It should be stressed that the absolute linkage between Pfiesteria and pollution has yet to be established, but the evidence seems quite strong.
It remains unknown why pollution may stimulate blooms of Pfiesteria more than others, but the answer may relate to the fact that this species can take up certain forms of organic nutrients, such as dissolved amino acids, that are found in pollution. Also, Pfiesteria can consume algae that have taken up the simpler, inorganic nutrients it is unable to utilize directly, such as nitrate.
Eggs of commercially important fish such as striped bass Morone saxatilus Walbaum and killifish Fundulus heteroclitus L. Pfiesteria piscicida also has been lethal to adult and larval shellfish, an effect that has been enhanced in the presence of finfish Burkholder et al. Adult scallops have died within minutes in the presence of finfish and actively toxic Pfiesteria , and adult blue crabs within days, of exposure to toxic Pfiesteria Burkholder et al. Larval eastern oysters Crassostrea virginica Gmelin and both larval and adult bay scallops Argopecten irradians Lamarck have been killed within minutes of exposure to toxic P.
If allowed direct contact, some toxic Pfiesteria strains have attacked and devoured the shellfish pediveliger larvae that previously had discarded their vela Figure 7 ; Springer Such attack is much less common for noninducible strains. In estuaries, the basic factors conducive to a toxic Pfiesteria outbreak, other than a robust Pfiesteria population with toxic strains, include the following: the presence of high densities of fish prey, particularly large schools of oily fish; poorly flushed, shallow water that is overenriched in nutrients, warm, and brackish; and abundant phytoplankton or other prey that serve as an alternate food source for Pfiesteria when live fish are not detected Burkholder and Glasgow During warmer seasons, the lower water column often contains a salt wedge, which consists of heavier saltwater from the ocean that underlies freshwater coming in from rivers Figure 3 ; Glasgow and Burkholder Benthic Pfiesteria populations active amoebae and cysts in nutrient-rich, organic sediments produce zoospores that become toxic in response to unidentified chemical cues from abundant fish, for example, surface-schooling Atlantic menhaden Figure 3.
Toxins from the zoospores narcotize and then kill the fish. Note that in the natural environment, neither toxic Pfiesteria spp. Although Pfiesteria can attack and kill fish in culture without other, interacting stressors, in estuaries they may more readily attack fish that are weakened by other factors Burkholder and Glasgow , Burkholder et al.
The pharmacological routes of human exposure to Pfiesteria toxins are distinct from most other dinoflagellate toxins, which have caused human illness and death primarily through consumption of toxin-contaminated seafood Falconer , Burkholder Pfiesteria did not appear to adversely affect people who ate seafood against our advice collected from areas where toxic outbreaks were in progress. However, the risk from consuming seafood from toxic Pfiesteria outbreaks cannot be ruled out until a reliable assay can be developed to test for Pfiesteria toxin in fish tissues Wright , Fairey et al.
Moreover, when the water from a fish-killing culture is filtered to remove cells of some Pfiesteria strains, the remaining toxin typically kills fish for only 3—8 hours, indicating that the toxin s is labile and highly unstable in water Burkholder and Glasgow , Moeller et al. Therefore, shortly after a Pfiesteria -related fish kill ends in an estuary within less than 24 hours , the area should be safe for human use.
The data, although preliminary, were available in and were taken into consideration in forming Maryland's policy for reopening affected areas to fishing and recreation.
As an extra precaution, areas were reopened 3 days after fish disease and death were no longer evident Magnien et al. Thus, based on sparse information, seafood may not be a major route for human exposure to Pfiesteria toxin see more recent data in Springer suggesting a potential seafood route. Additional evidence, from laboratory staff exposures, indicated that people were at risk of serious health impacts if they sustained water contact or inhaled aerosols where fish were diseased or dying and actively toxic Pfiesteria populations were present Glasgow et al.
Toxins from a few other dinoflagellate species are known to be released into the air from cells broken by wave action along beaches, and they have caused respiratory problems when inhaled by humans and dogs e. Somewhat analogously, laboratory workers became ill after inhaling aerosols from fish-killing Pfiesteria cultures.
Ten of 12 affected staff in several laboratories had worked with dilute concentrations, from to 13, toxic zoospores per mL, of Pfiesteria in fish-killing mode Burkholder et al.
The others had worked with higher cell densities that were still within field range: 90, cells per mL, versus up to , cells per mL reported at estaurine fish kills Glasgow et al. The subjects experienced burning skin and a tingling sensation during or following contact with the water from such cultures.
More seriously, Pfiesteria was the first dinoflagellate linked to production of aerosolized substances that seriously affect the human nervous system. Inhalation of the air over fish-killing cultures was related to symptoms that included blurred vision, burning skin and eyes, acute respiratory difficulty, muscle cramping, nausea, vomiting, severe headaches, and profound memory dysfunction Glasgow et al. The memory dysfunction was an inability to create new memory, apparantly similar to an Alzheimer's-like suppression of short-term memory and learning ability.
For days to weeks following exposure, several laboratory personnel could recognize words individually but could not form sentences, perform simple arithmetic, or remember more than the last words of a sentence directed to them. The most seriously affected person in our laboratory, who is a highly intelligent researcher, managed only a 7-year-old's reading level for 3 months after exposure and required reading lessons at first to help regain reading ability.
This person recovered normal cognitive function about 3 months after exposure to the toxic cultures Glasgow et al. For two others who were affected, long-term memory was compromised for several weeks, during which time they could not remember their names or where they lived. All the affected laboratory personnel were relatively young, mostly in their 20s or 30s, when they suffered these health impacts following repeated exposure to the dilute, fish-killing Pfiesteria cultures.
Certain symptoms have recurred in some individuals, especially following strenuous exercise. More chronic problems, such as auto immune reactions or both, are suspected to be related and have been ongoing for up to 8 years in several cases Schmechel and Koltai The data from the laboratory cases were presented to the North Carolina state health director and his staff at a formal meeting in the spring of , in the hope that the officials would evaluate the potential for health problems from Pfiesteria for people who use North Carolina's estuaries.
We also conveyed information from anecdotal accounts of fishermen who unknowingly had been in toxic Pfiesteria outbreaks. These people experienced nausea, burning skin and eyes, vomiting, joint and muscle pain, and severe headaches; some also described losing consciousness and finding themselves lost in estuaries they had fished since childhood. Lingering complaints included chronic infections, respiratory problems, complete lapses in memory of events that had occurred minutes before, and other disorientation.
When we had asked the National Oceanic and Atmospheric Administration NOAA; Beaufort, NC, and Charleston, SC and other federal agencies about recommended safety protocols for research with actively toxic Pfiesteria , we were informed that no federal regulations or guidelines were available for safety procedures in research with toxic algae.
The officials advised us that standard laboratory practices wearing a lab coat and gloves were adequate and used by their personnel in research with other toxic algae. When we informed university safety personnel that a person had been hurt while working with toxic Pfiesteria cultures in our laboratory, a small biohazard biosafety laboratory 3 BSL 3 facility was constructed for our use.
However, the facility proved to have defective air flow, which led to a second person being seriously hurt Glasgow et al. We then suspended all research with toxic Pfiesteria for about a year and a half, until an improved biohazard BSL 3 facility was completed Burkholder et al. Over that period, we learned of 10 others who had been affected, including people from three laboratories elsewhere, which strengthened the evidence that toxic Pfiesteria can cause human health impacts. A site visit and detailed evaluation of our laboratory's safety protocols were mandated by NOAA which, in an unusual action, had suspended funding of a small grant to our laboratory because of uncertainties about the extent of the problem.
The panel found our laboratory safety protocols satisfactory and supported NCSU's decision to require biohazard BSL 3 facilities for research with toxic Pfiesteria. NOAA required us to formally agree to use such facilities before further grant funding was released to our laboratory, and advised other granting agencies to follow a similar course.
Thus, as our knowledge about Pfiesteria developed, we were required to use biohazard BSL 3 facilities in recognition of the connection Glasgow et al. Such caution proved to be prudent as well as necessary. The improved biohazard BSL 3 facility prevented exposure to aerosols from toxic Pfiesteria cultures, and no one else in our laboratory was hurt. The most critically needed information about Pfiesteria was, and remains, the identity of its toxin s.
The toxin must be identifiable and quantifiable in order to address all of these objectives: determining whether seafood is unsafe to eat because of toxin contamination; assessing the extent to which people have been exposed to toxic Pfiesteria ; developing improved early warning systems to protect people from such exposure; and understanding the modes of action by which the toxin s impact human health.
This lack of information has seriously affected every facet of Pfiesteria science in both North Carolina and the Chesapeake Bay area, and it has been the greatest impediment to progress on the issue. Although we sought specialists to analyze the toxin s from our fish-killing Pfiesteria cultures, the few who agreed to begin to examine it gave the research low priority, in part because modest funding was available to support the research.
Three days after receiving 1 L of culture, they isolated a heat-stable, water-soluble fraction from the culture with potent fish-killing activity. The data were presented in several scientific forums, and results were corroborated by an independent laboratory Fairey et al. Toxin purification remained seriously impeded, however, because isolating enough of the highly unstable toxin for purification and identification proved more expensive than available funding could support.
Identification of dinoflagellate toxins typically requires many years. For example, brevetoxins are more amenable to analysis than Pfiesteria toxin because they are stable, lipid soluble, and produced in mass quantity by plant-like dinoflagellates that can be grown in simple media, without need of biohazard III facilities or live fish.
Nevertheless, it took about 20 years to purify brevetoxins and fully identify their chemical structures Falconer , Hallegraeff et al. From the initial isolation work with toxic Pfiesteria culture, an assay was developed to detect the water-soluble Pfiesteria toxin in laboratory cultures. Production of water-soluble toxin material for analysis by NOS-Charleston became the central focus of our research team before the toxic Pfiesteria outbreaks in Maryland Fairey et al.
However, toxin assays cannot reliably detect Pfiesteria toxin from estuarine samples until sufficient quantity of purified toxin becomes available for use as standard in the assay.
Thus, there was no reliable toxin assay available for use in diagnosing toxic Pfiesteria outbreaks in North Carolina, or Chesapeake Bay in When Pfiesteria was first implicated in fish kills in North Carolina, it allayed some of the concern building since the mids about many fish kills of unknown cause. However, because many toxic dinoflagellates contaminate seafood with their toxins Falconer , the seafood industry viewed publicized information about Pfiesteria as an economic threat Diaby Studies also showed that Pfiesteria can be stimulated by nutrient pollution Burkholder et al.
Nutrient over-enrichment of the affected North Carolina estuaries comes from many sources, such as stormwater runoff, sewage treatment plants, row crop agriculture, and swine and poultry feed operations Glasgow and Burkholder , Mallin et al. The potential for adverse human health effects from toxic Pfiesteria exposure was also problematic for tourism and coastal development Figure 8 , as has occurred with outbreaks of other toxic algae Burkholder Subsequent criticism of the validity of the published Pfiesteria research had long-term impacts on public opinion and influenced later treatment of the issue by state and federal authorities Paolisso and Chambers Complaints of disorientation, memory loss, burning eyes, burning skin, respiratory difficulty, nausea, and vomiting were conveyed to state and local health officials by people who had been exposed to fish kills that were confirmed to have involved toxic Pfiesteria Burkholder and Glasgow , Burkholder et al.
Such health problems were also described by 32 of 89 participants in an epidemiological questionnaire that was administered by state health officials Morris , McGeehin The participants had been in the toxic outbreak areas for minutes to hours.
However, clinical evaluations were not performed to discern whether they manifested cognitive impairment, with the exception of three people who were examined 6—9 months after the exposures. By that time, their symptoms could not be conclusively related to exposure to the toxic outbreaks Morris The potential for health impacts from exposure to toxic Pfiesteria was also dismissed on the basis of a health questionnaire administered to fishermen long after fish kills had subsided therefore, in the absence of actively toxic Pfiesteria ; Griffith , Lewitus et al.
Moreover, the health status of those exposed was based on reports from coastal physicians who had no diagnostic tool for relating symptoms to toxic Pfiesteria exposure Smith and Music An evaluation by an independent, scientific panel, requested by the governor of North Carolina, thus concluded that insufficient data were available from to to evaluate the potential for human health effects from toxic Pfiesteria exposure in North Carolina estuaries Wright In , potentially toxic strains of P.
Potentially toxic strains of this dinoflagellate had also been documented from the Patuxent Estuary on the western shore of the Chesapeake Burkholder et al. In fall and early spring , local fisherman suspected Pfiesteria of causing fish disease in the Pocomoke Estuary in Maryland, but the water samples were not tested with live fish in standardized fish bioassays; instead, they were tested using algal assays and, not surprisingly, Pfiesteria was not detected MDNR In late spring , we first examined samples from the Pocomoke Estuary that were sent by commercial fishermen, and we informed Maryland officials that the samples contained toxic Pfiesteria strains.
Fish bioassays and scanning electron micrographs SEMs of water samples collected later that spring and analyzed by our laboratory also indicated that toxic P. These samples were later confirmed as P. We served on a technical committee that first met in early August to provide guidance for Maryland environmental agencies on fish disease in the Pocomoke. Because the Pocomoke receives pollution from various sources MDNR , we cautioned the officials that there very likely were many other factors in the estuary, such as pathogens in leachate from poultry wastes or other sources, that could promote fish disease.
Less than a week later, the Pocomoke sustained a major fish kill with characteristics that suggested toxic Pfiesteria involvement, and within another week we confirmed the presence of actively toxic populations of Pfiesteria -like dinoflagellates. Clones of these organisms were toxic to fish in repeated, standardized fish bioassays, and SEMs and molecular probes verified that the organism involved in all four toxic outbreaks was P. All other species that resembled Pfiesteria in the samples were found not to be toxic in fish bioassays.
After considering this information, the governor of Maryland chose to take extra precautions protecting human health. The efforts taken by the governor and his staff to assess the situation and the evidence, to build scientific consensus, to clinically determine whether serious human health impacts could be sustained from exposure to a toxic Pfiesteria outbreak under field conditions, and to act with long-range vision to improve water quality protection e.
Maryland officials later obtained additional evidence in support of their decision to follow our diagnosis on the presence of actively toxic Pfiesteria in the four toxic Pfiesteria outbreaks Rublee et al. In other efforts to validate that research, a consensus group of officials and scientists from the Environmental Protection Agency, the Centers for Disease Control and Prevention CDC , NOAA, 10 states, and several academic institutions formally recommended that research be focused on known toxic Pfiesteria species rather than on look-alike species that have not been toxic to fish under ecologically relevant conditions P ICWG A national science panel later reevaluated Pfiesteria research for the CDC and also recommended a directed focus on known toxic Pfiesteria species rather than on look-alike taxa for which there is no evidence of similar toxicity by live or sonicated cells at field densities toward fish Samet et al.
Funding constraints of laboratories with demonstrated expertise have continued to seriously impede progress in Pfiesteria toxin production and analysis.
Therefore, assays to reliably detect Pfiesteria toxin from natural samples—the analytical tools that are critically needed by the CDC to conduct a meaningful, multistate epidemiological study, and by North Carolina and Maryland officials to design improved early warning systems to detect toxic Pfiesteria activity and thereby minimize human exposure—remain to be developed.
During the 4 years since the Maryland toxic Pfiesteria outbreaks, NOS-Charleston has been the only research group to publish Pfiesteria toxin data that were obtained following appropriate quality control and assurance procedure especially, use of toxic Pfiesteria cultures that were cross-corroborated by independent specialists as toxic strains of Pfiesteria spp.
Fairey et al. In mid the NOS-Charleston—based research team finished purification of a water-soluble neurotoxin from our Pfiesteria toxic culture material for chemical identification J. Ramsdell and P. Consensus by a panel of mid-Atlantic experts in support of the data for potential stimulation of Pfiesteria by nutrient pollution Boesch provided the basis for Maryland's governor and legislature to pass the strongest regulations for nonpoint pollution control in the nation, including mandatory nutrient management practices for agricultural operations by State of Maryland , Magnien Linkages between Pfiesteria and nutrient pollution under some environmental conditions were also supported by a national panel of scientists who met at the request of North Carolina's governor Wright and, later, by a national panel of scientists charged by the CDC to reevaluate the published literature on Pfiesteria Samet et al.
Samet et al. With funding support from the US Department of Agriculture USDA , EPA, and NOAA, many coastal states developed strengthened programs to improve nonpoint pollution control, monitor harmful algae in their regions, and assess chronic impacts of various stressors on fish health. The EPA and NOAA also have organized helpful workshops and provided publications for the citizenry scientists and nonscientists on Pfiesteria and other harmful algae.
Environmental education has been expanded in many states, with greater overall national focus on water quality issues. Spin-off initiatives have been many, and among the most encouraging were joint efforts by the USDA and the EPA to improve control of nonpoint pollution from concentrated animal operations, increased efforts by the poultry and swine industries to create value-added products from their wastes, and efforts to remove additional poultry wastes from the Delmarva peninsula State of Maryland Several important steps were taken in North Carolina to alter state policy governing Pfiesteria.
The environmental and health agencies developed an early warning system to test for toxic Pfiesteria at fish kill or disease events, and a plan to clinically evaluate people exposed to in-progress fish kills shortly after they are exposed, when the clearest available diagnostic, cognitive impairment, is detectable Glasgow et al. Support for Pfiesteria research and for environmental education programs was also strengthened Anderson and Stubbs It remains important to consider Pfiesteria in its proper context.
Many toxic dinoflagellates and other pathogenic microbes, including various species that have caused more serious health impacts than Pfiesteria Falconer , Burkholder , inhabit estuaries. Like most pathogenic microbes, Pfiesteria spp. Overall, the Pfiesteria issue has helped many people realize that water quality, fish health, and human health are strongly linked. Like many harmful algae Falconer , Pfiesteria outbreaks are sporadic Burkholder and Glasgow , Burkholder et al.
We hope that, beyond the short-term environmental and socioeconomic impacts of fish kills, beyond the progress realized in the two states that have had to confront toxic Pfiesteria outbreaks, and beyond the advances made in various other states as well as federal agencies to understand and protect fish and human health, this issue will eventually leave a more lasting legacy through strengthened efforts to manage and protect the quality of our nation's rivers, estuaries, and coastal waters.
Allen I. Master's thesis. Anderson N. Stubbs H. Several states have set up Pfiesteria hotlines, listed on the following page. Swimming, boating, and other recreational activities in coastal waters are generally safe.
Do not go into or near the water in areas that are closed by the state. Most species of algae are not harmful. Algae are the energy producers at the base of the ocean's food web, upon which all other marine organisms depend. Scientists call such events "harmful algal blooms. Some harmful algal blooms, like toxic Pfiesteria outbreaks, can cause detrimental effects when the microbes are at low concentrations in the water and cannot be visibly detected.
In other cases, like certain red and brown tides, harmful effects occur when the algae reach high concentrations that discolor the water. Some kinds of algal blooms are harmful because the algae produce one or more toxins that poison fish or shellfish, and can pose human health risks when people come in contact with affected waters. These toxic algal blooms may also kill seabirds and other animals indirectly as the toxins are passed up the food chain.
Certain kinds of these toxic algal blooms can cause human health problems via contaminated seafood, like Ciguatera Fish Poisoning, Amnesic Shellfish Poisoning, and Paralytic Shellfish Poisoning. However, there is no evidence that Pfiesteria-Telated illnesses are associated with eating fish or shellfish. Most algal blooms are not toxic, but they are still considered harmful if they reduce the amount of light or oxygen in the water, consequently killing sea grasses, fish or other marine life.
Pfiesteria is not a virus, fungus, or bacterium. It is not contagious or infectious, and cannot be "caught" like a cold or flu. Any human health problems associated with the microbe stem from its release of toxins into river and estuarine waters. Preliminary evidence suggests that exposure to Pfiesteria toxins in the air, water, or fish at the site of an outbreak can cause skin irritation as well as short-term memory loss, confusion, and other cognitive impairments in people.
It has been shown that similar human health effects can be caused by exposure to Pfiesteria toxins in a laboratory setting.
However, there is no evidence that illnesses related to Pfiesteria are associated with eating fish or shellfish.
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