History of Toxic Pfiesteria in North Carolina Estuaries from 1991 to the Present

The fish kills for which Pfiesteria became well known began in North Carolina, when very little research had been conducted on this unusual dinoflagellate. North Carolina's Albemarle-Pamlico Estuarine System, the epicenter of toxic Pfiesteria outbreaks, is the second largest estuary in area on the US mainland and the most important fish nursery ground on the US Atlantic Coast (Burkholder and Glasgow 1997, Mallin et al. 2000). As a conservative estimate, the state had sustained 48 toxic Pfiesteria outbreaks by 1997, involving more than a billion fish in an area more than 100 km2 (Burkholder et al. 2001a). These events had occurred nearly every summer beginning in 1991, when the organism was first recognized as an estuarine, fish-killing agent (Burkholder et al. 1992, 2001a, Burkholder and Glasgow 1997). In 1997, 50,000 fish died in a small area of the Chesapeake Bay from toxic Pfiesteria, and press coverage of the event was like an explosion. In the same summer, 1.2 million fish died during toxic Pfiesteria outbreaks in Albemarle-Pamlico estuaries, a 4-hour drive south of Washington, DC; those deaths went virtually unmentioned. North Carolina was the first state to encounter toxic Pfiesteria, and the knowledge gained there, especially about toxic Pfiesteria outbreaks and health impacts on laboratory workers (Burkholder et al. 1992, 1995, Burkholder and Glasgow 1995, 1997, Glasgow et al. 1995), benefited Maryland officials, who were challenged to act quickly and decisively. They evaluated and rapidly verified the role of toxic Pfiesteria in the Chesapeake Bay outbreak (MDNR 1998). Maryland was the first state from which people who reported neurocognitive, respiratory, and other symptoms from environmental exposure were clinically evaluated within a short period (1–3 weeks) after being exposed (Grattan et al. 1998). Maryland was also the first state to address the Pfiesteria problem by making significant advances in legislation for protection of water quality (State of Maryland 1998). Congressional attention following the toxic Pfiesteria outbreaks in Maryland led to the appropriation of many millions of dollars to federal agencies to research and manage toxic Pfiesteria outbreaks, resulting in excellent progress in some areas and setbacks in others. Here we examine the history of toxic Pfiesteria outbreaks before the four in Chesapeake Bay and a few aspects of the aftermath, from the perspective and experience of our research in the Albemarle-Pamlico Estuarine System with high toxic Pfiesteria activity. An important part of the Pfiesteria story is how North Carolina—with 98% of the Pfiesteria problem—subsequently moved to strengthen water resource protection, environmental education, and support of Pfiesteria research, actions that would not have been possible without the events that unfolded in Chesapeake Bay. The Pfiesteria story began in 1988 with the death of some fish held in brackish aquaria at the College of Veterinary Medicine, North Carolina State University (NCSU). We were asked by fish pathologists to help characterize an unknown microbial contaminant from the fish cultures. The microbe resembled many other benign, estuarine dinoflagellates (Figure 1), but the timing of its appearance in the aquaria raised the suspicion that it had caused the death of the fish. The small dinoflagellates were abundant in water samples taken when fish became lethargic, developed open bleeding sores, and hemorrhaged. Shortly after the fish died, however, the dinoflagellates seemed to “disappear,” by forming dormant cysts or other stages that left the water column and attached to fish or settled to the bottom of the aquaria. When more fish were added to the aquaria, the pattern was repeated, and higher dinoflagellate densities were attained (Burkholder et al. 1992). From that accidental contamination, we first learned of the existence of a small, apparently toxic dinoflagellate exhibiting rapid, predatory behavior in attacking and killing fish prey (Burkholder et al. 2001b). We began to conduct many experiments that tested, then verified, its toxicity to fish (Burkholder et al. 1995, Burkholder and Glasgow 1997). But the pathologists had obtained fish from all over the world and did not know which fish, from which geographic source, had carried the toxic dinoflagellate. Therefore, basic questions remained did this organism it of killing fish in The Albemarle-Pamlico Estuarine System the nursery ground area by fish from to is an important estuary for fish on the Atlantic (Figure Mallin et al. 2000). from the by the for this of water is on and to many estuaries, it from and Burkholder Mallin et al. 2000). In of the the and fish without known of summer and from the the that the for that of was (Burkholder 1998). with gained from the accidental of fish from at the state environmental and from the US for the first of the we developed a research to examine the organism was and toxic at estuarine fish We obtained water samples from a of about million Atlantic in the The samples were taken the was in when most fish were but not of water samples a abundant that were in appearance to the contaminant from the College of Veterinary samples taken than from a many fish at the few When tested, the water samples were to the same of toxic organism as the contaminant (Burkholder et al. 1992). the microbe had in the estuary as it had in the aquaria and to in a estuarine fish and and of the by other et al. we not the organism had been a would not that was we it the dinoflagellate for its appearance in the water in with fish by its (Burkholder et al. 1992). The known dinoflagellate had as a fish-killing the to that it a and of toxic dinoflagellate et al. The organism was Pfiesteria in of the research on dinoflagellates many about the of et al. Burkholder and Glasgow 1997). We developed in dinoflagellate in our laboratory et al. but we to our with other we as an quality in and in all toxic dinoflagellate laboratory that over a of to at or higher (Burkholder et al. The organism is in brackish of to water is than and water is about on the but it fish in and in the of (Burkholder et al. 1995, 2001a, Burkholder and Glasgow 1997). We that the organism the first known of a with behavior (Burkholder et al. 1992, our research had verified the of toxic Pfiesteria from the of south and to (Burkholder et al. 1995, Burkholder and Glasgow in Chesapeake Bay (Figure et al. In we first to a second toxic in water samples from North Carolina during fish kills (Burkholder and Glasgow 1997, Glasgow et al. but the became to in toxic of toxicity in over been reported for toxic of other toxic and it is to an of the (Burkholder et al. 2001a). we had of the second first to as Pfiesteria that were and toxic to fish. the and toxicity with in we the second Pfiesteria Glasgow Burkholder et al. in of the who of toxic dinoflagellate impacts on many that Pfiesteria, the would of had with and impacts (Burkholder et al. 2001a, 2001b). other toxic have been reported many but and have been as toxic to fish fish Burkholder and Glasgow 1997, et al. Burkholder et al. Therefore, at the toxic Pfiesteria (Burkholder et al. 2001a, the appearance of its small or was a of was the first dinoflagellate known to have cysts or dormant stages that the cysts of an of (Burkholder et al. 1992, Burkholder and Glasgow 1995, et al. nearly all other known or dinoflagellates with that the this dinoflagellate is or it prey (Burkholder and Glasgow 1995, 1997, et al. Pfiesteria act like a it was the first toxic dinoflagellate to fish prey (Burkholder et al. 1992, Burkholder and Glasgow 1995, 1997). Pfiesteria is also to in it as more than stages or not that the and the water column (Burkholder and Glasgow 1997, Burkholder et al. Glasgow et al. 2001a). with as well as is the most known for dinoflagellates (Figure and Burkholder et al. and the first that was reported for a toxic (Burkholder et al. 1992, Burkholder and Glasgow 1995, et al. by some have been as Pfiesteria, developed for of and (Burkholder et al. 2001a, Glasgow et al. and stages of Pfiesteria have been by et al. et al. 2000). Pfiesteria in have to is to an of in other Burkholder et al. 2001b). to of Pfiesteria as to at of (Burkholder et al. 2001b). the stages of Pfiesteria have been as a to the of some many other of toxic from estuarine and a in toxic to that apparently to in toxic in the of fish (Burkholder et al. 2001a, The toxic and or benign, in behavior fish, as for of and to and other environmental (Burkholder et al. 2001b). research on toxic in the to questions about fish and health (Burkholder and Glasgow 1997). we a fish (Burkholder et al. 1995, Burkholder and Glasgow 1997, et al. 2000). The for toxic than (Burkholder et al. 1995, et al. 1995, Burkholder and Glasgow 1997, et al. Burkholder et al. The toxic toxic or that of toxicity to fish but from fish for or not in Burkholder and Glasgow 1997, Burkholder et al. 2001a, The environmental that in nearly all toxic In was the first dinoflagellate to to in the of fish or and (Burkholder et al. 1992). from some toxic fish, and those have also been to fish when held in to with the fish prey (Burkholder and Glasgow 1997, 2000). In the of fish, toxic of Pfiesteria of other and as well as (Burkholder and Glasgow 1997). toxicity that to fish at stages 2000). of toxic that on other than fish fish for that the dinoflagellates were not toxic when the fish were from the fish (Burkholder and Glasgow 1997). In when with fish as toxic of have been to every and every more than and that have been (Burkholder et al. 1995), with of 2000). of have all but have not been to in the of in conducted of our toxic have been obtained from kills of Atlantic fish from the during and summer, and to in with abundant for and in not toxic Pfiesteria act to other of the estuarine prey that from to and (Burkholder and Glasgow The Albemarle-Pamlico Estuarine System is to for Pfiesteria Burkholder and Glasgow 1997). The water the that by Pfiesteria to fish that the water as fish that in the and by In fish in areas with abundant the the of the fish and the with or in the of fish, would a of for stages (Figure Burkholder and Glasgow 1997). Pfiesteria by as by research conducted in that became important to Maryland in the Chesapeake Bay toxic Pfiesteria outbreaks and in water quality to Pfiesteria (State of Maryland 1998). The of Pfiesteria the estuarine from and to and (Figure Burkholder and Glasgow 1995, 1997). in had not been for or in toxic Pfiesteria in and (Burkholder and Glasgow 1997). Pfiesteria as a by the from that it when fish not Pfiesteria in a and to for to in its et al. Pfiesteria with when by as and which in or and other (Burkholder and Glasgow 1997, et al. of the North Carolina toxic Pfiesteria outbreaks occurred in estuarine for which high from as or (Figure Burkholder et al. 1995, 1997, Burkholder and Glasgow 1997). were not for the other but also occurred in a in many fish had been held in a small, (Burkholder et al. 1995, Burkholder and Glasgow 1997). The of Pfiesteria is before it possible to the of in by the of on toxic of Pfiesteria had been in laboratory experiments to some (Burkholder et al. 1992, Glasgow et al. 1995, Burkholder and Glasgow 1997). about toxic Pfiesteria also in the and of the Chesapeake Pfiesteria in have or have well but for a short sustained other as a (Burkholder and Glasgow 1995, 1997). fish and toxic as as but toxic on prey for more than a few many Pfiesteria on than those on fish, but toxic Pfiesteria also have et al. which not in we to toxic Pfiesteria as with As for most toxic the of a role in to et al. Burkholder et al. 2001a). for toxic and of Pfiesteria fish or to water samples from an fish area (Burkholder and Glasgow 1997, Burkholder et al. toxic Pfiesteria dormant stages or cysts when from fish during at an estuarine fish especially during to for fish added to toxic to and the water column of then evaluated to were toxic at the estuarine fish (Burkholder et al. of prey other than fish not of estuarine samples to Pfiesteria was in the fish Pfiesteria toxic when fish. water samples taken from fish with prey than fish added as to of toxic Pfiesteria (Burkholder et al. Pfiesteria that were very in toxic or more without fish to to an and that dinoflagellates that in samples toxic of Pfiesteria for prey and high toxic Pfiesteria to in and is not When a of is to a or in the is by that that and of prey dinoflagellate to in toxic Pfiesteria were fish In of fish prey of toxic These then within a short period toxic and (Burkholder et al. research that toxic of Pfiesteria from samples by fish in fish (Burkholder et al. 1995, et al. 1995, Burkholder and Glasgow 1997, et al. Burkholder et al. The most of toxic Pfiesteria and within that and (Burkholder et al. 1992, Burkholder and Glasgow 1997). fish or that or as well as or bleeding or within to when fish exposed to Pfiesteria densities than to to those of estuarine fish or events (Figure Burkholder et al. 1995, Burkholder et al. 2001a, Glasgow et al. 2001b). some toxic and have developed in by Pfiesteria were in with fish and to the or were from fish by a which (Burkholder and Glasgow 1997). Pfiesteria have and impacts as well as impacts on exposure to toxic Pfiesteria by a or exposure to toxic Pfiesteria over to that fish became more to by those that et al. Burkholder et al. 2001a). The that Pfiesteria the fish which is by the in fish to to of (Burkholder 1998). also of the which is in the and is by Pfiesteria and its et al. of the would a problem fish in the of et al. 2000). of important fish as and have not during or after exposure to toxic Pfiesteria the possible in exposed fish (Burkholder Pfiesteria also been to and an that been in the of (Burkholder et al. 1995, 2000). have died within in the of and toxic Pfiesteria, and within of exposure to toxic Pfiesteria (Burkholder et al. and and have been within of exposure to toxic when the dinoflagellates were within to (Burkholder et al. 1995, 2000). some toxic Pfiesteria have and the that had (Figure 2000). is for In estuaries, the basic to a toxic Pfiesteria other than a Pfiesteria with toxic the the of high densities of fish of water that is in and and abundant or other prey that as an for Pfiesteria when fish not (Burkholder and Glasgow 1997). the water column a which of from the that in from (Figure Glasgow and Burkholder 2000). Pfiesteria and in that toxic in to from abundant fish, for Atlantic (Figure from the and then the fish. that in the toxic Pfiesteria other act fish health by Pfiesteria, microbial or exposure to water with a and other Pfiesteria and fish in without in more fish that by other (Burkholder and Glasgow 1997, Burkholder et al. The of exposure to Pfiesteria from most other dinoflagellate which have caused and death of Burkholder 1998). Pfiesteria did not to people who our from areas toxic outbreaks were in the from from toxic Pfiesteria outbreaks a developed to for Pfiesteria in fish et al. when the water from a fish-killing is to of some Pfiesteria the kills fish for that the is and in water (Burkholder and Glasgow 1997, et al. Therefore, after a fish in an estuary than the area for The were in and were taken in forming for areas to and As an areas were after fish and death were et al. Glasgow et al. 2001b). on not a for exposure to Pfiesteria more in a from laboratory that people were at of health impacts sustained water or fish were or and toxic Pfiesteria were et al. that for exposure water and was obtained by et al. 1998). from a few other dinoflagellate known to the from by and have caused when by and et al. 2000). laboratory workers became after from fish-killing Pfiesteria cultures. of in had with from to toxic of Pfiesteria in fish-killing (Burkholder et al. 1995, Glasgow et al. The had with higher densities that were within to reported at fish kills et al. The and a during or following with the water from cultures. Pfiesteria was the first dinoflagellate to of that the of the over fish-killing was to symptoms that and and et al. The was an to to an of and to following laboratory but not or more than the of a to The most in our who is a a for after exposure and at first to help about after exposure to the toxic et al. who were was for during which not or the laboratory were in or when health impacts following exposure to the fish-killing Pfiesteria cultures. symptoms have in some especially following as or to and have been for to in and The from the laboratory were to the North Carolina state health and at a in the of in the that the would the for health from Pfiesteria for people who North Carolina's We also from of who had been in toxic Pfiesteria These people and and and some also and in had in of events that had occurred and other of the who in did without making to Pfiesteria, health after in estuarine to our knowledge of health impacts from with of toxic Pfiesteria, in with the state health we the for actions that on the of health during toxic Pfiesteria When we had asked the and and and other federal agencies about for research with toxic Pfiesteria, we were that federal or were for in research with toxic The that laboratory a and were and by in research with other toxic When we that a had been with toxic Pfiesteria in our a small laboratory was for our the to have which led to a second being et al. We then all research with toxic Pfiesteria for about a and a an was (Burkholder et al. that we learned of who had been people from which the that toxic Pfiesteria health and of our were by in an unusual had of a small to our laboratory of about the of the The from and the of as well as state The our laboratory and to for research with toxic to to before was to our and other agencies to a as our knowledge about Pfiesteria we were to in of the et al. with toxic Pfiesteria and to as well as The exposure to from toxic Pfiesteria and in our laboratory was The most about Pfiesteria and the of its The and in to address all of is to of the to which people have been exposed to toxic to people from and the of by which the of every of Pfiesteria in North Carolina and the Chesapeake Bay and it been the to progress on the we to the from our fish-killing Pfiesteria the few who to to examine it the research in part was to support the before the Chesapeake Bay outbreaks, we began with at and from the of the of after of a from the with fish-killing activity. The were in and were by an laboratory et al. remained however, of the for and more than of dinoflagellate many more to than Pfiesteria and in by dinoflagellates that in without of or fish. it about to and et al. From the with toxic Pfiesteria an was developed to the Pfiesteria in laboratory cultures. of for by became the of our research before the toxic Pfiesteria outbreaks in Maryland et al. Pfiesteria from estuarine samples of for as in the was for in toxic Pfiesteria outbreaks in North Carolina, or Chesapeake Bay in When Pfiesteria was first in fish kills in North Carolina, it some of the the about many fish kills of unknown many toxic dinoflagellates with the about Pfiesteria as an was on the that is when people of a or other toxic dinoflagellate The to to the of an all is when it from also that Pfiesteria by (Burkholder et al. 1992, Glasgow et al. 1995, et al. 1995, Burkholder and Glasgow 1997, et al. et al. of the North Carolina from many as and and and Burkholder Mallin et al. 2000). The for health from toxic Pfiesteria exposure was also for and (Figure as occurred with outbreaks of other toxic (Burkholder 1998). of the of the Pfiesteria research had impacts on and of the by state and federal and of and were to state and health by people who had been exposed to fish kills that were to have toxic Pfiesteria (Burkholder and Glasgow 1997, Burkholder et al. 2001a). health were also by of in an that was by state health 1997). The had been in the toxic outbreak areas for to were not to with the of people who were after the that symptoms not to exposure to the toxic outbreaks The for health impacts from exposure to toxic Pfiesteria was also on the of a health to after fish kills had in the of toxic et al. and the health of those exposed was on from who had for symptoms to toxic Pfiesteria exposure and 1998). An by an by the of North Carolina, that were from to to the for health from toxic Pfiesteria exposure in North Carolina 1998). In toxic of were first in Chesapeake Bay by on a of the on et al. toxic of this dinoflagellate had also been from the on the of the Chesapeake (Burkholder et al. and were as toxic in fish (Burkholder and Glasgow 1997, Burkholder et In and 1997, Pfiesteria of fish in the in but the water samples were not with fish in fish were not Pfiesteria was not (MDNR 1998). In 1997, we first samples from the that were by and we Maryland that the samples toxic Pfiesteria and of water samples that and by our laboratory also that toxic was in the samples were as by other et al. et al. Burkholder et al. 2001a, We on a that first in to for Maryland environmental agencies on fish in the the from (MDNR we the that very were many other in the as in from or other that fish than a the sustained a fish with that toxic Pfiesteria and within we the of toxic of of were toxic to fish in repeated, fish and and verified that the organism in all four toxic outbreaks was et al. 2000). In toxic Pfiesteria was other that resembled Pfiesteria in the samples were not to toxic in fish this the of Maryland to The taken by the and to the and the to to clinically health impacts sustained from exposure to a toxic Pfiesteria outbreak and to act with to water quality protection State of Maryland in Burkholder and Glasgow and in this of Maryland obtained in support of to our on the of toxic Pfiesteria in the four toxic Pfiesteria outbreaks et al. et al. et al. 2000). In other to that research, a of and from the the for and and that research on known toxic Pfiesteria than on that have not been toxic to fish Pfiesteria research for the and also a on known toxic Pfiesteria than on for which is of toxicity or at fish et al. of with have to progress in Pfiesteria and Therefore, to Pfiesteria from that by the to conduct a and by North Carolina and Maryland to to toxic Pfiesteria and to the the Maryland toxic Pfiesteria outbreaks, been the research to Pfiesteria that were obtained following quality and of toxic Pfiesteria that were by as toxic of Pfiesteria et al. Burkholder et al. 2001a, et al. In the research of a from our Pfiesteria toxic for and by a of in support of the for of Pfiesteria by the for and to the for in the for by (State of Maryland Pfiesteria and some environmental were also by a of who at the of North Carolina's by a of by the to the on Pfiesteria et al. et al. also the of our research on toxic Pfiesteria and of toxic our fish with the of with other toxicity and of Pfiesteria to fish in the and of Pfiesteria to fish in support from the US of and many developed to in and impacts of on fish The and also have and for the and on Pfiesteria and other been in many with on water quality have been and the most were by the and the to of from by the and to from and to from the (State of Maryland 1998). the million to North Carolina in the Albemarle-Pamlico to help and it fish and toxic Pfiesteria outbreaks as the for that important were taken in North Carolina to state on all toxic Pfiesteria outbreaks was added to the fish 1998). The environmental and health agencies developed an to for toxic Pfiesteria at fish or and a to clinically people exposed to fish kills after when the is et al. 1995, et al. 1998). for Pfiesteria research and for environmental was also and 2000). important to Pfiesteria in its toxic dinoflagellates and other that have caused more health impacts than Pfiesteria Burkholder most Pfiesteria for but not for and health the Pfiesteria many people that water fish and health many Pfiesteria outbreaks (Burkholder and Glasgow 1997, Burkholder et al. 2001a). We the environmental and impacts of fish the progress in the that have had to toxic Pfiesteria outbreaks, and the advances in other as well as federal agencies to and fish and this a more to manage and the quality of our estuaries, and of stages of Pfiesteria and toxic for that from a toxic of toxic of the toxic Pfiesteria in US toxic of Pfiesteria have been fish The Albemarle-Pamlico Estuarine System, Chesapeake and the the known toxic Pfiesteria have been during fish the same to the Chesapeake Bay outbreaks, our research verified the of toxic of in the of Burkholder et al. 1995), of the et al. 1995), the Chesapeake Bay Burkholder et al. 1995), many in North Carolina (Burkholder et al. 1995, Burkholder and Glasgow in (Burkholder and Glasgow 1997, Glasgow et al. and Bay in (Burkholder et al. in the Pfiesteria been more et al. but have not been for the Chesapeake Bay outbreaks, toxic of Pfiesteria have been verified from and toxic Pfiesteria to fish kills in the the and that in summer, during of and water from in the water water in the water The resulting water have and The water by water from is high in from the and is from in to the bottom The water column also is higher in and abundant and abundant from In the more bottom water is in and and from of and that have settled fish caused by toxic Pfiesteria when of fish as Atlantic to and act as that by and Pfiesteria These Pfiesteria to that fish and from Pfiesteria and been with as that for to of a toxic of Pfiesteria that by its to a and the without a within of the that for of a toxic of Pfiesteria to The was in water with at a of Pfiesteria in and all were which with were than of the in all exposed to toxic following of exposure to a of toxic Pfiesteria Burkholder et al. Atlantic with a from a toxic Pfiesteria outbreak on the North also to as during toxic Pfiesteria outbreaks (Burkholder et al. 1995, Burkholder and Glasgow 1997). for toxic of after being taken from a fish-killing in and a that had its was taken after the Pfiesteria were added to the with the In this within than the had most of the for the 2000). for from North Carolina about the Pfiesteria in 1995, from toxic Pfiesteria outbreaks, in the following a Atlantic were and from a toxic outbreak in the million fish were a were in during that and many and and about Pfiesteria and water quality in North Carolina from to the toxic Pfiesteria outbreaks in for of the fish and for the toxic and of were during fish and were within following 100 with in Glasgow et al. were of about few to the in all four and and and Burkholder et al. for the of the fish and for the toxic and of were during fish and were within following 100 with in Glasgow et al. were of about few to the in all four and and and Burkholder et al. for the