PFIESTERIA PISCICIDA: Ichthyotoxic Estuarine Dinoflagellate
Professor D. Rahni
Env. Law 802
December 7, 1999
This paper reports on and discusses a newly-discovered (1991)
and classified single-celled organism called Pfiesteria
piscicida and its morphologically-related organisms (MRO's) (as
yet unclassified).
In the early 1990’s, coastal estuaries in
North Carolina experienced massive fish kills of unknown origin.
Subsequently these fish kills were attributed to Pfiesteria by
Dr. JoAnn Burkholder of North Carolina State University.
Since their discovery, these MRO’s have been found in coastal
waters from the Delaware Bay to the Gulf Coast of Alabama, and
have caused fish kills and human health problems in North
Carolina and Maryland.
They are part of a growing phenomenon
broadly referred to as Harmful Algal Blooms (HAB’s), which is
affecting fish and mammal health in coastal areas worldwide.
While their causes are not conclusively proven to be related to
human effects on the environment, there is persuasive evidence
suggesting a strong link between algal blooms and excessive
nutrient presence: nitrogen and phosphate pollution in coastal
waters.
What Is It?
Pfiesteria is an ichthyotoxic dinoflagellate.
Dinoflagellates
are aquatic, motile, single-celled planktonic organisms.
They
move in the water by means of the whiplike appendages (flagella)
that they use for swimming in some of their life stages.
Ichthyotoxic means harmful to fish, and is derived from the
Greek word for fish (ichthys).
There are nearly two thousand species of dinoflagellates, which
take many different forms. Many dinoflagellates, like
Pfiesteria, are considered “harmful algae” based on their toxic
effects during algal blooms like the so-called “red tides”.
The
term “harmful algae” refers to true algae, which are primitive
plants that make chlorophyll and get energy by photosynthesis,
as well as to various single-celled creatures that look like
algae but behave differently.
Pfiesteria combines some of the attributes of true algae, some
of the characteristics of other toxic dinoflagellates, and
aggressive predatorial behavior towards fish prey. Pfiesteria's
name is derived from the name of a well-respected phycologist,
Dr. Pfiester, the Latin word for fish (piscis) and the Latin
suffix for killer (-cida) (e.g. fratricide, matricide
and patricide).
In 1984, there were 22 known species of toxic
dinoflagellates; in 1997 there were more than 60.1
Life Cycle
Pfiesteria differs from its cousins by virtue of its complicated
life cycle.
It can change into at least 24 different forms,
depending on environmental conditions and the amount of prey
organisms in the water.2
uM.
1
It can vary in size from 4 uM to 450
These shape and size changes can take place in as little as
Newsday, NY, October 7, 1997, p.C3, quoting Dr. JoAnn Burkholder.
10 minutes.3
With no fish prey in the surrounding water, the
cells stay either in the form of amorphous amoebae that stay in
the bottom mud, cysts of various sizes that remain dormant,
protected by a tough coating of armor-like “thecal” plates, or
swimming cells known as nontoxic zoospores.
When fish arrive, these zoospores become toxic, and cysts and
amoebae change to nontoxic zoospores which in turn become toxic.
The toxic zoospores emit toxins that act to stun the fish and
damage their skin.
They also feed on the substances generated
by the damage inflicted on the fish skin.4
And they reproduce
asexually, producing gametes that can combine to create
planozygotes.
The planozygotes and gametes join in the feast on
the dead or dying fish.
Once the fish is dead, the Pfiesteria
return to the form of amoebae that feed on the carcass.
If no fish are present in the water, but algae are present, the
toxic zoospores and gametes revert to nontoxic zoospores and
amoebae feeding on the algae. If algal prey is abundant, the
nontoxic zoospores may multiply, creating more potentially-toxic
attackers should fish swim into the area.5
“The Lurking Perils of Pfiesteria”, Scientific American, August 1999, pp.
42-49, Burkholder, J.M.
3 Ibid.
4 “Fish lesions in the Chesapeake Bay:Pfiesteria-like dinoflagellates and
other etiologies”, Maryland Medical Journal, 47 (3), pp. 106-112, Kane, A.S.,
Oldach, D., and Reimschuessel, R.
2
5
NCSU Aquatic Botany Laboratory Pfiesteria piscicida Page
http://www.Pfiesteria.org/pfiest.html#CYCLE
Pfiesteria is also capable of consuming algal cells and stealing
their chloroplast, a phenomenon called cleptochloroplasty.6
This
gives Pfiesteria the capacity to produce energy from sunlight.
In the absence of fish prey, Pfiesteria may also assume the form
of cyst-like zygotes.
Where Is It?
In 1988, a doctor at the veterinary school of North Carolina
State University called JoAnn Burkholder.
Tanks of fish used
for testing were dying with no visible cause.
After a tank of
fish died, the lab workers regularly cleaned out and dried the
tank. But when fresh water and new fish were added to the tank,
6
Ibid., fn.3.
the same cycle happened.7
Dr. Burkholder, a botanist by
training, began to study the water to see what could be causing
the deaths.
She and her assistant isolated a dinoflagellate
that seemed to flourish in the presence of fish and to cause the
fish to die.
Three years later, during a massive fish kill in the Pamlico
Estuary on North Carolina’s coast, Dr. Burkholder looked at a
water sample from the Pamlico River and realized it contained
the same dinoflagellate that had apparently been causing the
death of the lab fish.
After consulting with staff at North Carolina’s Department of
Environment, Health and Natural Resources she learned that
samples of water taken from fish kills in North Carolina since
at least 1985 had contained the same dinoflagellate.8
Since 1991, Pfiesteria or its MRO’s have been identified as
being present at fish kills all along the east coast of the
United States, in Florida and on the Gulf Coast of Alabama. From
1992 to the present, Pfiesteria were identified in the lower
Eastern Shore of the Chesapeake Bay in Maryland, and in various
fish mortalities at laboratories and culture ponds at fish
farms.9
Pp can survive a bath in concentrated sulfuric acid or ammonium hydroxide,
thirty-five days of dessication, or almost two years of dormancy. Watch out
for killer algae, E–the Environmental Magazine, V. 7, Mar/Apr 1996, pp. 1519, Mulvaney, K.
8 And the Waters Turned to Blood, by Rodney Barker, Simon & Schuster 1997
9 Ibid., fn.4.
7
Pfiesteria have a wide salinity tolerance and a wide temperature
tolerance.10
They prefer calm waters, retreating into their non-
toxic cyst stage in water that is not brackish.
There is
considerable scientific consensus that there is a strong
connection between MRO blooms and overloads of nutrients like
nitrogen and phosphorus.11
This may be stimulation directly or
indirectly by creating an abundance of algal prey.12
A Maryland Blue Ribbon Citizens Action Commission Report (the
“Cambridge Consensus”) and a subsequent report by a group of
aquatic ecologists, chemists, biologists and other scientists at
the University of North Carolina’s Water Resources Research
Institute (the “Raleigh Report”) both conclude that nutrient
loading increases the risks of toxic outbreaks of Pfiesteria and
MRO’s and the resulting fish kills.13
In the Cambridge Consensus, scientists estimated that
agriculture accounts for 70 percent of the nitrogen pollution
and 83 percent of the phosphorus pollution on the Maryland
shore.
And in Florida, an outbreak of a dinoflagellate-induced
fish kill, by an MRO named Cryptoperidiniopsis, was linked to
the release, by state and federal water managers, of billions of
Congressional Research Service Report for Congress: “Pfiesteria and
Related Harmful Blooms: Natural Resource and Human Health Concerns”, 12/8/97,
Buck, E.H., Copeland, C., Zinn, J.A., and Vogt, D.U.
11 A study of the relationship between inorganic and organic nitrogen and the
growth of dinoflagellates in eutrophic conditions found a striking
relationship between the availability and uptake of urea and the outbreak of
dinoflagellates. In 25 sampling periods in estuarine ponds with temperatures
between 5 and 30 degrees Centigrade, urea concentrations greater than 1.5 uM
co-occurred with dinoflagellates 75 percent of the time. Abstract of a
report to conference in Santa Fe, Feb. 1999, Gilbert, P.M., Terlizzi, D.M.,
Lomas, M.W., Fan, C.
12
“Pfiesteria piscicida and other Pfiesteria-like dinoflagellates:
Behavior, impacts and environmental controls”, Limnology and Oceanography,
42(5, part 2), 1997, p. 1052-1075, Burkholder, J.M. and Glasgow, H.B., Jr.
13 Baltimore Sun, Jan. 31, 1998, p. 1B
10
gallons of polluted floodwater from Lake Okeechobee into the
Indian River.14
Nutrient loading as a cause of toxic outbreaks is especially
significant in light of the rapid growth of feedlot operations
in both Maryland and North Carolina in the last decade.15
North
Carolina is one of the largest swine and poultry-producing
states in the USA.
In 1996, the state housed 9.8 million hogs.
In 1997, the poultry industry consisted of approximately 60
million turkeys and 680 million chickens.16 In 1995 a toxic
outbreak of Pfiesteria occurred in North Carolina after five
major spills from lagoons of hog waste released an estimated 30
million gallons of nutrient-rich waste into the Neuse River in
North Carolina17.
And in Maryland, approximately 620 million chickens are raised
on the eastern shore of the Chesapeake Bay each year.18
In the
Pokomoke River watershed in Maryland, the amount of chicken
manure spread on fields as fertilizer every year equals the
sewage output of a city of 1 million people.19
There is some scientific support for the hypothesis that North
Carolina’s fish kills have been more significant (numbering in
Fort Lauderdale Sun-Sentinel, March 19, 1998, p. 1A
In the Neuse and Cape Fear River Basins of North Carolina, in the 1980’s 2
million livestock head were counted in 21,000 operations, and 15 years later
the number reached 8.3 million head in 6000 operations. This speaks to not
just growth but also to concentration. “Coastal management”, Water Environment and Technology, v. 9, Aug. 1997, pp. 63-65, Doll, B.
16 Comparative effects of poultry and swine waste lagoon spills on the quality
of receiving streamwaters, Journal of Environmental Quality, v. 26 Nov./Dec.
1997, pp. 1622-31, Mallin, M.A., Burkholder, J.M., McIver, M.R.
17 “Impacts to a coastal river and estuary from rupture of a large swine waste
holding lagoon,” Journal of Environmental Quality, v. 26, Nov./Dec. 1997, pp.
1451-66, Burkholder, J.M., Mallin, M.A., Glasgow, H.B., Jr.
18 “Cell from Hell”, Sierra Magazine, 84 (1), Jan./Feb. 1999, p. 34, Guynup,
S.
14
15
the billions rather than the thousands or millions, as in
Maryland) because the Chesapeake Bay is deeper than the
Albemarle-Pamlico Estuary system, and more frequently and
thoroughly flushed by the ocean as a result of its wider opening
to the Atlantic.
The greater depth may reduce the growth of
phytoplankton that feed Pfiesteria, and may make the Bay waters
less calm.20
In addition, the Outer Banks, a system of barrier islands along
the North Carolina coast, prevents the flushing out of the
nutrients and pollutants from inland waters that contribute to
the conditions under which Pfiesteria thrives.
While Pfiesteria seems to be present in some form all along the
coastal estuaries of the Atlantic, it is not always actively
causing fish kills.
Certain conditions need to be present
before the dinoflagellate begins to emit toxins that kill fish
and affect humans.
The ideal conditions include a combination
of brackish waters, high concentrations of phytoplankton that
feed Pfiesteria, and large schools of fish that trigger toxin
production by Pfiesteria.
What Does It Do?
Unlike some other toxic dinoflagellates, Pfiesteria does not
accumulate in the food chain, harming fish and humans who ingest
it.21
Nor does it seem to proliferate and suffocate fish by
building up in gills.
St. Louis Post-Dispatch, September 22, 1997, p. 1A.
The Baltimore Sun, August 29, 1997, p. 17A.
21 Blooms of the Alexandrium species of dinoflagellates cause shellfish to
become toxic. People who eat shellfish that carry saxitoxins can suffer
paralytic shellfish poisoning (PSP), which can lead to respiratory paralysis.
19
20
Instead, Pfiesteria responds to the trigger of large numbers of
fish by releasing toxins that stun the fish, lower their immune
resistance and damage the fish skin.
numbers.22
The fish die in large
Pfiesteria, in some of its forms, feeds on the dead
and dying fish in a process called myzocytosis, in which
zoospores, gametes and planozygotes attach with an extended
peduncle and suction the interior cytoplasm and organelles.23
In addition, Pfiesteria toxins can harm people.
People who are
exposed to the toxin on their skin or who inhale the toxin in
aerosolized form can be beset by severe neurological deficits
that fade, more or less, with time and the end of the exposure.
Symptoms have ranged from narcosis, eye irritation, respiratory
distress, stomach cramping and vomiting, epidermal lesions,
cognitive impairment, fits of rage and short-term memory loss.24
There is some indication that immune responses may be hampered,
in both humans and in fish.25
Fish health
Ciguatera is another species that can lead to poisoning of humans who eat
affected fish, bringing episodes of gastroenteritis and neurological
symptoms. Red tides of Gymnodinium breve along the Florida coast have caused
deaths to seabirds and marine mammals like the manatee. G. breve can also
cause respiratory and eye irritations in humans who are exposed to it in sea
spray, its aerosolized form. Two other kinds of poisoning by fish
consumption, diarrhetic and amnesic shellfish poisoning, are also the result
of the toxins carried by fish who eat harmful algae. “Pfiesteria, ‘The
Cell from Hell,’ and Other Toxic Algal Nightmares,” Clinical Infectious
Diseases 1999; v. 28, pp. 1191-1198, Morris, J.G., Jr.
22 “In 1991, we lost over a billion fish.
They were burying them on the beach
with a bulldozer. And in 1995 we lost well over ten million.” Rick Dove,
Riverkeeper for the Neuse River in North Carolina, quoted in “Cell from
Hell,” Sierra Magazine, ibid. fn. 18.
23 Ibid., fn.12.
24 Ibid., fn.12.
25 Ibid., fn.2.
Pfiesteria responds to unidentified fish excreta by swimming
toward fish prey and emitting multiple toxins.26
The toxins are
as yet unidentified, except that one is water-soluble and one is
fat-soluble.27
The toxins narcotize the fish, causing erratic
swimming patterns and distress, bleeding, difficulty obtaining
sufficient oxygen and extensive lesions and death.28
The fishes’
epidermal tissue and osmo-regulatory functions are destroyed or
severely impaired.29
Pfiesteria toxins also can make the fish vulnerable to diseasecausing bacteria and fungi.30
Finally, as noted above, various
stages of Pfiesteria feed on the cells of the dead and dying
fish.
Within hours of a toxic outbreak, following the death of
most of the fish, Pfiesteria’s toxic stages transform into nontoxic forms.31
Recent tests also indicate that fish exposed to low
concentrations of toxic Pfiesteria suffered from white blood
cell counts 20 to 40 percent lower than normal, suggesting that
Ibid., fn.12.
“Strategies for environmental monitoring of toxin producing phantom
dinoflagellates in the Chesapeake,” Maryland Medical Journal, May 1998,
47(3), p. 113-119.
28 “A new ichthyotoxic dinoflagellate: cause of acute mortality in aquarium
fishes,” The Veterinary Record (1993), v. 133, p. 96-97, Noga, E.J., Smith,
S.A., Burkholder, J.M., Hobbs, C., Bullis, R.A.
29 Ibid., fn.12.
30 In particular, the fungus Aphanomyces can cause lesions and die-offs of
fish. The question of whether Pp or Aphanomyces causes the extensive lesions
commonly associated with Pp outbreaks appears to be somewhat contested.
“Fungus, not Pfiesteria, blamed for fish lesions,” Environmental News
Network, October 6, 1998. And ibid., fn.4.
31 Ibid., fn. 27.
26
27
Pfiesteria toxins may compromise the functioning of the immune
system. Eggs of striped bass and other fish fail to hatch,
shellfish larvae are killed and young bay scallops lose the
ability to fully close their shells.32
Human health
Pfiesteria and its MRO’s cause Estuary Associated Syndrome in
humans.
Lab workers with heavy exposure, watermen and a
waterskier are some of the victims of the syndrome. The most
common symptoms of EAS are lack of concentration, forgetfulness,
inability to learn new information, information overload, skin
lesions or burning sensations and possible immune impairment.33
Unlike other toxic dinoflagellates, Pfiesteria does not appear
to build up in seafood and harm people who eat the seafood.
People get ill who get toxin-laden water on their skin or who
breathe aerosolized toxins in the air over the areas where fish
are hurt or dying from Pfiesteria.
Studies of watermen exposed to Pfiesteria bore out the symptoms
reported by the three lab workers who were exposed to water
containing Pfiesteria toxin by skin and aerosol contact in a lab
setting.34
Neuropsychologic testing showed severe memory
Ibid., fn.2.
For hair-raising descriptions of the human health effects, see And the
Waters Turned to Blood, ibid. fn.8, for its discussions of JoAnn Burkholder
and Howard Glasgow’s bouts of EAS. Dr. Burkholder has had pneumonia 16 times
since she had Pp-caused EAS, in 1995.
34 “Learning and memory difficulties after environmental exposure to waterways
containing toxin-producing Pfiesteria or Pfiesteria-like
32
33
impairment, including recall for verbal and visual information,
and abnormal attention spans.35
Suggestions that Pfiesteria EAS
complaints were psychosomatic have been rejected.36
In addition, studies conducted in which rats were exposed to
Pfiesteria toxins showed significant deficits in their ability
to learn new mazes, which were more pronounced when the tests
were conducted in a chamber without sound attenuation,
indicating susceptibility to distraction.37
What Is Being Done?
Due to the increase in the number of HAB’s, there is
considerable political activity that attempts to reduce nutrient
runoff from agricultural facilities like hog feed-lots and
chicken farms.
The problems to be addressed include non-point
source run-off of fertilizer and waste, and spills from waste
dinoflagellates,” The Lancet, August 15, 1998, v. 352, p. 532-538, Grattan,
L.M., Oldach, D., Perl, T.M., Lowitt, M.H., Matuszak, D.L., Dickson, C.,
Parrott, C., Shoemaker, R.C., Kauffman, C.L., Wasserman, M.P., Hebel, J.R.,
Charache, P., Morris, J.G., Jr.
35 “Neurologic symptoms following Pfiesteria exposure: case report and
literature review,” Maryland Medical Journal, May 1998, 47(3), p.120-123,
Bever, C.T., Jr., Grattan, L.M., Morris, J.G.
36 “A critical review of the Pfiesteria hysteria hypothesis,” Maryland
Medical Journal, May 1998, 47(3), p. 133-136, Greenberg, D.R., Tracy, J.K.,
Grattan, L.M.
37 “Persisting learning deficits in rats after exposure to Pfiesteria
piscicida,” Environmental Health Perspectives, v. 105 (1997), p. 1320-1325,
Levin, E.D., Schmechel, D.E., Burkholder, J.M., Glasgow, H.B., Jr., DeamerMelia, N., Moser, V.C., Harry, J.G.
And “Pfiesteria Toxin and Learning
Performance,” Neurotoxicology and Teratology, 21(3), p. 215-221 (1999),
lagoons.
Increased protection for wetlands and limits to
farming in floodplains are two strategies being used.
Some
activity centers on the state level, some on the federal level.
In North Carolina, state regulators proposed a plan in 1996 to
reduce by 30 percent the amount of nitrogen runoff in various
land use zones.
Some combination of riparian buffers, nutrient
management, drainage or other best management practices were
proposed to reduce the nutrient load from farmland.38
A
moratorium on new hog farms was put in place the year after
massive swine waste lagoon spills into the Neuse River.
Farmers
in North Carolina protested, as did commercial fishers.39
In Maryland, the governor appointed a panel to assess the
dangers.
The panel strongly urged reductions in the use of
manure as fertilizer, and the Maryland Assembly considered bills
to accomplish that reduction.
Farmers found such proposals
“alarming” and organized to oppose them, in vain.40
Other Atlantic coast states, including Virginia, Delaware, West
Virginia, Pennsylvania, South Carolina and Florida, are
cooperating in research and data-sharing, and several are
setting up task forces and research units.41
Levin, E.D., Simon, B.B., Schmechel, D.E., Glasgow, H.B., Jr., Deamer-Melia,
N.J., Burkholder, J.M., Moser, V.C., Jensen, K., Harry, G.J.
38 Ibid., fn.14.
39 “The water will take care of itself,” quoting a fisherman in Pamlico
County, North Carolina. The Boston Globe, November 30, 1998.
40 The Baltimore Sun, January 4, 1998, p.1B.
41 Ibid., fn.10.
Considerable amounts of grant monies are being funneled into
Pfiesteria research, including more that $2.4 million in state
and federal funds from the Maryland and from the National
Oceanic and Atmospheric Administration.42
Federally, the EPA announced a proposed strategy to cope with
the problem of agricultural runoff from non-point sources,
including permitting under the Federal Water Pollution Control
Act.
The system of TMDL’s instituted by the states under the
Section 303(g) of the FWPCA has been criticized for being poorly
designed, monitored
and enforced.
Other federal statutes with
potential impact include the 1987 Water Quality Act, section 319
(providing grants to states to develop non-point source
management programs, but not requiring implementation of
enforceable laws) and the 1990 Coastal Zone Management Act (each
coastal state required to develop a non-point source pollution
control program).43
In 1999, Congress passed 16 U.S.C. section 1451, the “Harmful
Algal Bloom and Hypoxia Research and Control Act of 1998,”
providing funding for research on HAB’s, which was referred to
the Senate Committee on Commerce, Science and Transportation and
heard from no more.
Congress also passed H.R. 2565, the
“Pfiesteria Research Act of 1997,” which appears to have died in
42
The Baltimore Sun, October 6, 1998, p.2B.
a different committee in the Senate.
Meanwhile the Senate
passed a bill called “The Atlantic Coast Toxic Microorganism
Environmental Remediation Act,” which was also referred to the
Committee on Environment and Public Works.
In 1998, the House
referred a bill entitled the “Farm Sustainability and Animal
Feedlot Enforcement Act” to the Committee on Transportation and
Infrastructure.
The many federal agencies whose program areas cover HAB’s,
including the EPA, the National Science Foundation, the
Department of Health and Human Services’ National Institute of
Health, the Department of Defense’s Office of Naval Research,
NASA’s Office of Earth Science, and the Department of Commerce’s
National Oceanic and Atmospheric Administration, are trying to
jointly fund research.
Research is continuing on all aspects of Pfiesteria and its
MRO’s, including human health effects, toxin identification,44
effective methods of identifying Pfiesteria-laden areas at risk
through gene probes and toxic bioassays and possible control
methods.45 Research is continuing on all aspects of Pfiesteria
“Reinventing Environmental Regulation: Back to the Past by Way of the
Future,” Environmental Law Reporter, July 1998, v. 28, p. 10361-10372,
Steinzor, R.I.
44 The Baltimore Sun, October 6, 1997, p.1A.
45 “Response of two zooplankton grazers to an ichthyotoxic estuarine
dinoflagellate,” Journal of Plankton Research (1995), 17(2), p. 351-363,
Mallin, M.A., Burkholder, J.M., Larsen, L.M., Glasgow, H.B., Jr.
43
and its MRO’s, including human health effects, toxin
identification,
effective methods of identifying Pfiesteria-
laden areas at risk through gene probes and toxic bioassays and
possible control methods.
Long Term Implications
The main concerns to scientists studying Pfiesteria are the
potential threat to viability of fish populations, human health
concerns, and the possible economic effects on tourism,
fisheries and recreation.
Estuaries are the nursery ground for
a wide variety of fish species.
If fish kills weaken immunity
and reduce breeding populations, it could affect the ability of
fish populations to recover.
Dr. Burkholder believes that HAB’s are clear evidence of the
increasing stresses on estuarine ecosystems from anthropogenic
effects.
She likens fish killed by MRO’s to canaries in a coal
mine, an early warning system that we would be foolish to
ignore.