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Pfiesteria and Related Harmful Blooms:
Eugene H. Buck, Claudia
Copeland, and Jeffrey A. Zinn
Donna U. Vogt, Analyst
December 8, 1997
What is Pfiesteria?
Congress, federal agencies, and affected states are seeking to better understand Pfiesteriapiscicida (a recently identified species of dinofiagellate) and related species, whose blooms release toxins that can harm fish and possibly human health under certain conditions. Although menhaden, an industrial fish used primarily in fishmeal and oil production, is the dominant species observed to have been killed by these organisms, consumers have reduced their purchases of Chesapeake Bay seafood after extensive media coverage highlighted toxic events. Both the water and lipid-soluble toxins of Pfiesteria and related species have been blamed for adverse health effects in people who have come in contact with affected waters.
Many scientists believe that nutrient enrichment of waters plays a role in Pfiesteria outbreaks, but the exact mechanisms are unclear. Some agricultural activities, especially large livestock facilities, are concentrated sources of nutrients, which can leach into ground and surface waters. In Maryland, phosphorous from these sources has attracted considerable attention, because it is often the limiting factor whose increase encourages blooms of aquatic organisms such as Pfiesteria. However, agricultural interests believe that this attention unfairly singles out agriculture, and they are investigating alternative explanations. Most agree that more investigation is required to develop a better understanding of the role of nutrient pollution. In affected watersheds, agricultural agencies and interests are both collecting information to characterize current farming enterprises and conservation accomplishments more fully and increasing staff and financial resources to work with farmers on reducing nutrient concentrations.
While individual states seek to address concerns and determine how to mitigate associated impacts, Congress and federal agencies are considering how best to assist state efforts. Federal and state governments have funded surveillance efforts as well as research into testing and characterization of the toxins and their effect on human health. Reauthorization of the Clean Water Act, which could occur in the 2nd Session of the 105th Congress, may give policymakers opportunities to consider what role that Act might play in addressing Pfiesteria-related and similar water quality problems. Legislative attention to research and related topics also could occur.
Although initially it appeared easy to assume that Pfiesteria or related organisms were the problem and that agricultural practices were the cause, state and federal agencies are examining a broad array of causes and remedies. One example of a broad approach to these problems is provided in the November 1997 report by the Blue Ribbon Citizen's Pfiesteria Action Commission to Maryland Governor Parris Glendening, which will be the basis for further actions by the Maryland Legislature.
Even with widespread implementation of several programs to protect and improve water quality in coastal waters, there has been an increase in the frequencies, virulence, and geographic extent of toxic blooms 1 of planktonic marine organisms, and increased biomass of non-toxic blooms has become apparent along the whole U.S. coastline, including Alaska and Hawaii, during the 1990s. So-called "red tides" by Gymnodinium dinoflagellates have caused fish and marine mammal mortalities offshore of many states, while increased algal growth off the mouth of the Mississippi River annually produces a massive anoxic zone, devoid of most marine life. While the problems of harmful blooms appear to be widespread and possibly increasing, this report focuses specifically on the more recent concerns with Pfiesteria-like species in the mid-Atlantic region. These concerns have attracted congressional interest
House subcommittee hearings, specific FYI 998 appropriations provisions, and as justification for several general legislative proposals.
Major fish kills have been attributed to Pfiesteria piscicida, a species of dinoflagellate (a group of aquatic, motile, single-celled, planktonic organisms), in North Carolina primarily in the estuaries of the Neuse and Pamlico Rivers) since the early 1990s. While a 1996 fish kill at a Maryland fish farm was associated with Pfiesteria piscicida, other Pfiesteria-like organisms have been identified in Maryland, Delaware, Virginia, South Carolina, and Florida. Other than the Maryland fish farm, however, scientists have not yet validated the reports of Pfiesteria in the wild in these other states. Dinofiagellate species similar to, and easily confused with, Pfiesteria have been identified in some of these areas, including the Pocomoke River in Maryland. Fish kills in these east coast estuaries usually were associated with hot summers and periodic, brief, heavy rains within the middle and lower portions of coastal river watersheds. Lesions on estuarine fish, particularly in menhaden, have been documented from New York to Florida since the early 1980s. Although some have suggested that instances of ulcerative mycosis (fungal lesions) in mid-Atlantic menhaden during the mid-1980s may have been caused or influenced by Pfiesteria like organisms, 2 this is conjecture and has not been proven. Because lesions are non-specific and can be caused by a number of mechanisms, lesions alone are insufficient to indicate Pfiesteria exposure.
It has been puzzling to some that no associated mortalities have been reported of animals (e.g., gulls, terns, cormorants, marine mammals, raccoons, turtles) that inhabit the same estuaries and may feed on dead or infected fish. In addition, no symptoms of respiratory distress, neuromotor function impairment, wasting, sores or lesions, or general unkempt appearance have been reported in these other animals, which would almost certainly have been exposed to any airborne toxins and contaminated water and/or ingested contaminated fish. This absence of symptoms raises questions about the virulence of the toxins as well as the range and duration of potential impacts, since dinofiagellate red tides have been observed to cause distress and mortality widely in affected ecosystems.
Pfiesteria piscicida, discovered in 1988 in a laboratory fish tank and formally identified and named in 1996, was identified from fish kill areas in the estuaries of the Pamlico and Neuse Rivers of North Carolina in 1991. Dr. JoAnn Burkholder, an associate professor at North Carolina State University, has focused much of her recent work on characterizing this organism. Pfiesteria piscicida has a complicated life cycle involving as many as 24 different physical forms, with the ability to transform quickly (i.e., within minutes to hours) from one form to another. While most forms are non-toxic, some life stages release toxins that have been blamed for fish kills and implicated in human illness in North Carolina. At least two different toxins have been identified as released by this organism, a fat-soluble toxin that causes skin lesions and a water-soluble toxin that is neurotoxic.
Identification of Pfiesteria-like organisms is difficult, requiring special treatment of the organism's cells and viewing under a scanning electron microscope (SEM). However, few laboratories have the equipment and experience necessary to perform this identification. A number of dinofiagellate species in possibly several genera -a "Pfiesteria complex" of morphologically similar species - may occur together and be responsible for the Pfiesteria-like fish mortality events. SEM has not always revealed the presence of Pfiestieria in samples identified as positive by toxicity bioassay procedures. 3 In addition, this organism's ability to transform quickly between non-toxic and toxic forms has made it difficult to identify the organism causing specific toxic events. Several similar species may act like Pfiesteria, inducing a positive response in toxicity bioassays, but are not recognizable as Pfiesteria under SEM. Several investigators, using SEM, suggest that some of the toxic events may be caused by dinoflagellates of a new unidentified genus, possibly related to Peridiniopsis. 4
Pfiesteria-like dinoflagellates exist over extensive environmental and geographic ranges. They have a wide salinity tolerance for both freshwater and seawater, as well as wide temperature tolerance. Optimum conditions for Pfiesteria and related species are shallow, brackish, slow-moving waters, typically found in estuaries; temperatures of about 75 degrees F; and an abundance of fish. These conditions change seasonally; hence, toxic outbreaks tend to occur in spring and summer months. Scientists believe that these organisms are present at all times in estuarine waters where they have been found, but become active, and potentially toxic, only under certain conditions.
Nutrient (nitrogen and phosphorus) enrichment of the waters may play a role in Pfiesteria outbreaks, but the mechanisms are unclear. For example, some scientists believe that, at certain points in its life cycle, Pfiesteria can be stimulated directly by dissolved organic nutrients derived from human and animal wastes (sewage and manure). Pfiesteria has been found in higher abundance near sewage outfalls. Others speculate that nutrients in sewage, manure, and land runoff encourage the growth of algae which are consumed by Pfiesteria, thus stimulating the organism's growth indirectly.
Some scientists believe that there is strong linkage between nutrient pollution and Pfiesteria outbreaks in at least some of the affected waters, but others are much less certain. Nutrients, by stimulating algae growth, may provide food for Pfiesteria, but linkages are not clearly understood. Because bacteria in the water break down algae, water becomes depleted of oxygen needed to sustain aquatic animals. As a result, waters in which Pfiesteria are found also are characterized by low dissolved oxygen levels. Some scientists believe that, at least in some cases, low dissolved oxygen levels may have caused fish kills and that Pfiesteria bloomed as a result of dying or dead fish in the water column. In such cases, Pfiesteria outbreaks are an indirect result of fish kills, rather than their cause. However, other scientists speculate that, in those waters, low dissolved oxygen levels may be due to the decomposition of dead or dying fish, and not the cause of the fish kill.
Another possibility is that certain toxic compounds, such as agricultural pesticides in the water, may stress fish populations, regardless of Pfiesteria. Some scientists are investigating whether various compounds in the water could promote the growth of certain types of algae, which may stimulate the growth of Pfiesteria. Another potential explanation being examined is that organic nutrients, many of which are naturally occurring (such as organic material flushed by storms from swamps and wetlands in the watershed), may play an equal or more important role than inorganic nutrients from fertilizers in stimulating Pfiesteria and other harmful blooms. Or, it may be that the relative amounts of different nutrients are what is important. Nearly all agree, however, that much more investigation is required to determine more conclusively what role, if any, nutrient pollution may play and, if so, at what stage or stages in the organism's life cycle. It is likely to take time to develop enough information to clearly implicate any individual factor or group of factors in the conditions which result in toxic outbreaks of Pfiesteria piscicida and similar organisms.
Scientists have postulated that schools of plankton-eating fish, such as menhaden, feed on abundant algae and other plankton that Pfiesteria also feeds upon and excrete or secrete a substance that triggers Pfiesteria to become active and toxic, especially in the absence of its preferred food. Of the two toxins released by Pfiesteria, a water-soluble neurotoxin stuns and paralyzes fish. This toxin also can be found in air close to the water. A second lipid-soluble toxin acts on the skin of the fish, causing the skin to dissolve. Fish exposed to either of these toxins may die, but toxic levels have not yet been identified. When fish were exposed to a concentrated extract of the water-soluble toxin in the laboratory, they became moribund in 2 to 3 seconds and died within 3 minutes. Apparently, both toxins dissipate a few hours after release.
Pfiesteria does not attach to the fish, but feeds upon the sloughing skin and blood. Lesions created by the dissolving skin cause a fish to lose its physiological integrity, rendering it susceptible to other secondary infections and osmoregulatory (water balance) disturbances. Opportunistic secondary infections by bacteria and/or fungi are likely to be the primary cause of deep sores, lesions, or ulcers.
In extreme cases, Pfiesteria-like organisms occur in such abundance that the toxins released cause major fish kills. Menhaden, an industrial fish harvested primarily for fishmeal and oil, is the fish species that has most often been affected. Other fish inhabiting these waters also are affected and include flounder, croakers, spot, and gar. Unverified estimates were as high as one billion fish, primarily menhaden, killed in the Neuse and Pamlico River estuaries, NC, during 1991 - 1993.
Very little research on the human health effects of Pfiesteria toxins has been conducted. At a multi-state workshop at the Centers for Disease Control and Prevention (CDC) in Atlanta, Georgia, at the end of September 1997, attendees agreed on clinical symptoms that characterize the adverse health consequences of exposure to Pfiesteria toxins. These clinical features include:
With these criteria and environmental qualifiers (e.g., 20% of a 50-fish sample, all of the same species, have lesions caused by a toxin), it is likely that Pfiesteria-related surveillance data can better track potential illnesses.
Pfiesteria toxins have been blamed for causing adverse health effects in people who have come in close contact with waters where this organism is abundant. Since June 1997, the Maryland Department of Health and Hygiene has been collecting data from Maryland physicians through a state-wide surveillance system on illnesses suspected of being caused by Pfiesteria toxin. As of late October 1997, illness was reported by 146 persons who had been exposed to diseased fish or to waters that were the site of suspected Pfiesteria activity. Many of these persons are watermen and commercial fishermen.
The strongest evidence of adverse human health effects so far comes from case studies of two research scientists who were both overcome in their North Carolina laboratory in 1993. They still complain of adverse effects on their cognitive abilities, particularly after exercising. Duke University Medical Center researchers conducted experiments on rats, which showed that the toxin appeared to slow learning but did not affect memory.
Maryland. In the summer of 1997, Governor Parris Glendening of Maryland, citing human health risks, closed almost all the estuaries where fish kills were observed. Meanwhile, Maryland officials advised against swimming and against eating fish with open, red sores in areas (e.g., the lower Pocomoke River estuary, King's Creek in the Manokin River watershed, and portions of the Chicamacomico River drainage) where researchers found potentially toxic dinoflagellates that could have caused lesions in fish.
Using funds from the National Oceanic and Atmospheric Administration (NOAA) and the Environmental Protection Agency (EPA), Maryland conducted two surveys to learn more about agricultural activities in the affected watersheds. The Maryland Department of Agriculture completed an assessment of agricultural activities 5 centered on best management practices (BMPs).6 This report was based on a survey of current activities and on-site visits to almost a quarter of all farms in the Pocomoke drainage. The results of this study are summarized below, in the discussion of agricultural issues. The University of Maryland conducted a companion study of agricultural nutrient management plans.
Maryland took other actions to address nutrient concerns. First, the state's Department of Agriculture offered financial assistance to encourage farmers to grow winter wheat cover crops. Cover crops can reduce soil erosion as well as incorporate phosphorous and other nutrients that are attached to soil particles and store them in plant materials; these stored nutrients become available to crops grown the following year.
Second, Maryland became the first state to apply successfully to the U.S. Department of Agriculture (USDA) to implement a Conservation Reserve Enhancement Program (CREP). The state had been developing this proposal for about a year; the proposal was adjusted to increase the emphasis on counties where excessive nutrient runoff was suspected after fish kills occurred in the Pocomoke River and neighboring watersheds. Vice President Al Gore, Agriculture Secretary Dan Glickman, and Governor Glendening signed a Memorandum of Agreement to implement this program at a widely publicized press conference on October 20, 1997. This program, discussed below, will allow farmers in approved counties to receive bonus rental payments when they enroll land in the Conservation Reserve Program, retiring it from production for a decade or longer if they apply certain conservation practices designed to reduce the movement of soil and nutrients into surface waters.
Governor Glendening added three positions in the state's Department of Agriculture to provide technical support to farmers and three positions in the Department of Environment to inspect farms and initiate any necessary regulatory enforcement to protect water quality in the affected watersheds. These new efforts to reduce nutrient pollution are in addition to efforts by Maryland, Virginia, Pennsylvania, and the District of Columbia, as signatories and participants in the Chesapeake Bay Program over the past 15 years, to reduce nitrogen and phosphorus loadings to the Bay. In particular, the states and the District agreed to a goal of reducing nutrient loadings to the Bay by 40% by the year 2000.7
Maryland officials took an active role in making a clear distinction that most Maryland seafood was harvested from areas unaffected by Pfiesteria and posed no concern for consumers. In addition, Maryland officials made statements to the effect that certain commercial crabbers were likely to be reimbursed for losses directly related to the closing of Maryland estuaries.
Researchers at Johns Hopkins School of Medicine and the University of Maryland, at the direction of Governor Glendening, examined 22 people exposed to Maryland waters thought to contain Pfiesteria, and 8 with similar backgrounds, but no contact with Pfiesteria, who served as a control group. It is unknown to which, if any, of the toxins these people may have been exposed. In September 1997, the medical team issued a preliminarily report that it was impressed with the collected medical histories of patient after patient noting acute problems with memory loss. These researchers concluded that the presence of Pfiesteria toxin in water could pose a health risk.
At the heart of the Maryland response are the activities of a blue-ribbon panel, appointed by Governor Glendening in mid-September 1997, which issued its final report to him on November 3, 1997. 8 The Commission made recommendations about reducing nutrient loadings from upland sites generally and from agriculture in particular, about responding to public health concerns, and about future research, monitoring, and assessment needs. For example, in responding to public health concerns, the Commission recommended that the State of Maryland should continue to maintain a central registry of all potential and confirmed cases of Pfiesteria-toxin poisonings. This registry could then be used to conduct further epidemiological studies. The Commission also recommended that physicians continue to report cases of possible Pfiesteria-linked illnesses, and that studies be conducted to better define the clinical and subclinical manifestations of varying degrees of exposure to Pfiestena toxins.
North Carolina. In North Carolina, both the General Assembly and state regulators imposed new planning and management requirements on agricultural operators to address nutrient overload and Pfiesteria problems with fish kills in certain waters, particularly the Neuse River. The state's Environmental Management Commission is seeking agreement on measures to achieve a 30% reduction in nutrient loadings to that river. Early in 1997, the North Carolina Department of Environment and Natural Resources issued guidelines and instructions for local health officials warning of possible dangers to swimmers and fishermen associated with Pfiesteria. In September 1997, the North Carolina Department of Health and Human Services established a medical team from university medical programs to evaluate North Carolina residents possibly exposed to Pfiesteria toxins, and opened a telephone hotline to gather information from people who believe they may have suffered from Pfiesteria-related health problems.
Virginia. Although Virginia officials closed a segment of the Lower Pocomoke River in Virginia, Governor George Allen believed more evidence of human health risks was needed and did not close segments of the Rappahannock River where lesions had been found on menhaden. He asked Virginia scientists to review the Maryland medical team findings, while Virginia's Health Commissioner announced that Virginia was creating an independent team of medical experts to assess Pfiesteria effects on human health. Governor Allen also ordered the Virginia Department of Health to create a Pfiesteria epidemiology research unit, transferred funds to the new unit, and designated money for the purchase of SEM technology to aid in species identification. Similar to Maryland, Virginia officials took an active role in making the distinction that most seafood was harvested from areas unaffected by Pfiesteria and posed no concern for consumers. The Virginia House of Delegates Committee on the Chesapeake Bay and Its Tributaries held a hearing on Pfiesteria and associated concerns in October 1997.
Other States. In early October 1997, Florida Department of Environmental Protection (DEP) officials announced that a special state task force was being created to increase understanding of Pfiesteria-like organisms (e.g., those identified in Florida's St. Johns River). In addition, Florida DEP scientists and laboratory facilities provided expertise and leadership in identifying Pfiesteria-like dinoflagellates from water samples submitted by other coastal states. Delaware officials organized a Pfiesteria Response Team to monitor areas where fish with lesions were reported. Delaware officials have sought to address consumer concerns over seafood safety, and have requested funding to reduce nutrients released by wastewater treatment facilities and contributed by urban runoff. South Carolina and Georgia officials are monitoring the situation, but have not taken any action since no outbreaks of Pfiesteria-like organisms have been reported in their waters.
Interstate Cooperative Efforts. On September 19, 1997, the Governors of Maryland, Virginia, Delaware, and West Virginia, and representatives from North Carolina, Pennsylvania, and the Clinton Administration met and agreed to conduct joint research and to share data on Pfiesteria-like organisms and events.
Elements of the Federal Response. In response to concerns raised by the State of Maryland, several federal agencies, including NOAA, EPA, USDA, the U.S. Geological Survey ~SGS), and the Department of Health and Human Services, have been involved in investigating the problem, providing financial and technical assistance, and conducting or coordinating research. No single agency has the lead in these efforts, but EPA and NOAA are coordinating activities of a number of agencies and departments. Their efforts have three related elements; coordinating research, responding to the states' needs for monitoring and assessment, and trying to prevent future outbreaks of Pfiesteria and other harmful blooms.
Coordinating a Federal Research Strategy. Many federal agencies are conducting research to increase understanding of the human health and environmental effects of Pfiesteria outbreaks and the environmental factors (nitrogen, phosphorus, and other factors) that may contribute to such events. Both of these research areas are believed to be critical to respond appropriately to Pfiestena outbreaks. EPA and NOAA are leading a multi-agency group to develop a federal research strategy for Pfiesteria and related organisms. This strategy will reflect the research that federal agencies are currently supporting, as well as identify needs and priorities for the future. According to EPA officials, the goal is to ensure that all research efforts (federal, state, and other) are shared and complementary, not redundant, and are addressing the key questions as quickly as possible. The national research strategy will focus on four areas:
This plan, to be reviewed by federal and state agencies and the academic community, is intended to provide a sound base from which to build control and mitigation strategies through various coastal management programs and thus to reduce and prevent future occurrences of harmfiil blooms.
EPA's Office of Research and Development is currently working on several fronts to shed light on how to prevent and control future outbreaks of Pfiesteria. EPA, NOAA, the National Science Foundation (NSF), and the Office of Naval Research are jointly funding the Ecology and Oceanography of Harmful Algal Blooms (ECOHAB) research program over a 3-year period. Recently initiated studies in the first round of this program are expected to contribute to a better understanding of harmful blooms, their effects on human health, and the role of nutrients on the growth of harmful blooms. Results of these studies may be useful in assisting resource managers in predicting where and when a toxic bloom may occur.
Further, in support of the Interagency Committee on Environment and Natural Resources (CENR), EPA also is participating in the National Environmental Monitoring and Research Initiative. This initiative includes a pilot project in the mid-Atlantic region which is designed to better document current nutrient levels in estuaries and improve understanding of the linkages among air, land, water, biota, and people.
Supporting State Responses to Toxic Pfiesteria Outbreaks. In response to the human health and environmental risks and impacts associated with marine biotoxins and harmful blooms, EPA, NOAA, and other federal agencies have been working with states to better understand and, ultimately, manage or respond to harmful blooms in general and, most recently, to Pfiesteria-complex organisms in particular. EPA, USDA, and other agencies are especially interested in what steps can be taken to reduce nutrient pollution, and prevent these toxic events and their effects.
A group, led by NOAA's Chesapeake Bay Program Office, is coordinating federal activities to help mid-Atlantic states respond to Pfiesteria outbreaks. This group, primarily composed of federal field office representatives, has identified a number of near-term activities believed to be critical to helping the states immediately, as well as other activities that will help over the longer term.
Reducing Nitrogen and Phosphorus Loadings from All Sources. Although research has not yet conclusively linked nitrogen and phosphorus with toxic outbreaks of Pfiesteria, many federal officials and scientists believe that there is a very strong association, based on the observed events. In addition, extensive research and strong evidence suggest that excessive nitrogen and phosphorus levels lead to other harmful blooms (some of which are toxic and harmful to human health), such as red and brown tides, and can also lead to low oxygen levels and fish kills. Thus, further reducing nitrogen and phosphorus levels in coastal waters is believed to be a high priority if risks to human health and the environment caused by Pfiesteria outbreaks and other harmful blooms are to be prevented.
However, because the sources of nutrient pollution are many and varied, federal officials recognize that solutions undertaken by water quality and resource managers also must be varied. EPA officials support nutrient reduction programs in several areas, including:
1 A "bloom" is an event involving extremely rapid population growth by a species of drifting (i.e., planktonic) aquatic organism. During a bloom, an organism that otherwise is seldom noticed because of its microscopic size may impart a color to the water (e.g., a "red" tide) by its abundance.
2 Fungal lesions may be a secondary opportunistic response to skin lesions caused by Pfiestieria toxins.
3 A toxicity bioassay involves placing a suspect water sample in an aquarium containing fish, and waiting to see if the dinoflagellate organisms reproduce and induce the characteristic lesions and death in the fish. This procedure may require as long as two weeks to complete. While a toxicity bioassay may confirm the toxicity of a sample, it may not be conclusive as to a cause and effect relationship between the organism in the sample and the toxic episode in the waterway coincident with sample collection.
4 Steidinger, Karen A. 'Pfiesteria piscicida, Other Pfiesteria Species, and Pfiesteria Like Species: A Question of Recognition and Toxicity." Informational handout prepared July 31, 1997, for the Pocomoke River Fish Health Technical Advisory Committee.
5 Maryland Department of Agriculture. Preliminary Characterization of Agriculture in the Pocomoke Watershed. Annapolis, MD: October 1997. 16 p.
6 BMPs are one or more conservation practices that are determined by the state water quality agency or its planning designee to be practical means for controlling point and non-point source pollutants at levels compatible with environmental goals.
7 Officials in these states expect to meet the phosphorus reduction goal, as a result of wastewater treatment plant improvements and bans on phosphate-containing detergents. Municipal and industrial plant controls also have led to reduced nitrogen loadings to the Bay, but officials believe that continued discharges from less well-controlled sources of nitrogen, including runoff from farms, lawns, and storm sewers, will prevent attaining the nitrogen reduction goal by the year 2000. Goodman, Peter S. and Todd Shields. "Not-So-Sick Bay; Despite Outbreak of Pfiesteria, Chesapeake Showing Signs of Improvement, Scientists Say." Washington Post, Oct.27, 1997, pp. B1, B7.
8 Blue Ribbon Citizen's Pfiesteria Action Commission. Final Report. Annapolis, MD: Nov. 3, 1997. 49 pp. plus appendices.
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