8
42 Scientific American August 1999 The Lurking Perils of Pfiesteria O n a hot, humid October af- ternoon in 1995, I stood in a gently rocking boat, watch- ing hundreds of thousands of bloody, dying fish break the mirrorlike surface of North Carolina’s Neuse Estuary, where the Neuse River mixes with salty water from the Atlantic Ocean. Rising up out of the river, writhing, the fish gasped for air, then became still, float- ing on their sides. They were mostly At- lantic menhaden, small fish that serve as food for many larger species valued by commercial fishermen. An occasion- al flounder, croaker or eel also bobbed on the surface. Seagulls lined the shores of the nearly eight square miles of kill zone; a feast was in the making. With my team from North Carolina State University (N.C.S.U.), I was col- lecting water samples from the area to try to determine the cause of the deaths. The bloody sores on the fish and their erratic behavior signaled a possible tox- ic outbreak of Pfiesteria piscicida, a sin- gle-celled microorganism that we had first seen in 1989 and had later linked to fish kills in several major estuaries. By the time this kill was over, 15 mil- lion silvery carcasses would carpet the water. We quickly completed our sampling and pulled anchor, knowing it would be unwise to linger if P. piscicida was the culprit (as our test results later indi- cated was the case). People who have had contact with this creature in its toxic state have suffered from a range of symptoms, among them nausea, res- piratory problems and memory loss so severe that it sometimes has been mis- taken for Alzheimer’s disease. The scene on the river was all too fa- miliar. In 1991 a billion fish died in the same way in this estuary. Since then, P. piscicida, occasionally with a closely re- lated but unnamed toxic species, has been implicated almost yearly in mas- sive fish kills in the estuaries of North Carolina (where it typically wipes out hundreds of thousands to millions of fish in a year) and in several smaller kills involving thousands of fish in Maryland waters of Chesapeake Bay. These two species are the first mem- bers of the “toxic Pfiesteria complex,” referred to hereafter as simply Pfieste- ria. They (or still other toxic species that look the same but have not yet been identified definitively) have now been found as well in coastal water- ways extending from Delaware to the Gulf Coast of Alabama, although they The Lurking Perils of Pfiesteria This minute creature has been implicated in dramatic fish kills and has hurt people. But its most publicized actions may not be the most damaging. More subtle effects are raising new concerns by JoAnn M. Burkholder DEPARTMENT OF BOTANY,NORTH CAROLINA STATE UNIVERSITY (N.C.S.U.) Copyright 1999 Scientific American, Inc.

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Page 1: The Lurking Perils of Pfiesteria

42 Scientific American August 1999 The Lurking Perils of Pfiesteria

On a hot, humid October af-ternoon in 1995, I stood in agently rocking boat, watch-

ing hundreds of thousands of bloody,dying fish break the mirrorlike surfaceof North Carolina’s Neuse Estuary,where the Neuse River mixes with saltywater from the Atlantic Ocean. Risingup out of the river, writhing, the fishgasped for air, then became still, float-ing on their sides. They were mostly At-lantic menhaden, small fish that serveas food for many larger species valuedby commercial fishermen. An occasion-al flounder, croaker or eel also bobbedon the surface. Seagulls lined the shoresof the nearly eight square miles of killzone; a feast was in the making.

With my team from North CarolinaState University (N.C.S.U.), I was col-lecting water samples from the area to

try to determine the cause of the deaths.The bloody sores on the fish and theirerratic behavior signaled a possible tox-ic outbreak of Pfiesteria piscicida, a sin-gle-celled microorganism that we hadfirst seen in 1989 and had later linkedto fish kills in several major estuaries.By the time this kill was over, 15 mil-lion silvery carcasses would carpet thewater.

We quickly completed our samplingand pulled anchor, knowing it wouldbe unwise to linger if P. piscicida wasthe culprit (as our test results later indi-cated was the case). People who havehad contact with this creature in itstoxic state have suffered from a rangeof symptoms, among them nausea, res-piratory problems and memory loss sosevere that it sometimes has been mis-taken for Alzheimer’s disease.

The scene on the river was all too fa-miliar. In 1991 a billion fish died in thesame way in this estuary. Since then, P.piscicida, occasionally with a closely re-lated but unnamed toxic species, hasbeen implicated almost yearly in mas-sive fish kills in the estuaries of NorthCarolina (where it typically wipes outhundreds of thousands to millions offish in a year) and in several smaller killsinvolving thousands of fish in Marylandwaters of Chesapeake Bay.

These two species are the first mem-bers of the “toxic Pfiesteria complex,”referred to hereafter as simply Pfieste-ria. They (or still other toxic speciesthat look the same but have not yetbeen identified definitively) have nowbeen found as well in coastal water-ways extending from Delaware to theGulf Coast of Alabama, although they

The Lurking Perils of PfiesteriaThis minute creature has been implicated in dramatic fish kills and

has hurt people. But its most publicized actions may not be the most damaging. More subtle effects are raising new concerns

by JoAnn M. Burkholder

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The Lurking Perils of Pfiesteria Scientific American August 1999 43

have not been linked to fish deaths out-side North Carolina and Maryland.

Over the past 10 years, my colleaguesand I have learned a great deal aboutPfiesteria’s life cycle and about the rea-sons for its proliferation and toxic out-breaks. We have also found it to be anastonishing creature, displaying proper-ties never before seen in dinoflagellates—the larger group of microorganisms towhich it belongs. Dinoflagellates, en-compassing thousands of species, gaintheir name from the whiplike append-ages (flagella) that they use for swim-ming in certain of their life stages.

Other unexpected findings haveprompted us to look beyond the float-ing dead fish to Pfiesteria’s additionaluntoward actions. Disturbingly, we haveseen that aside from killing many fish atonce, Pfiesteria can impair the health offinfish and shellfish in more subtle ways,such as by undermining their ability toreproduce and resist disease. These lessobvious effects could potentially de-plete fish populations more permanent-ly than acute kills do.

Pfiesteria is not alone in its quiettreachery. Work by many investigatorshas also turned up insidious activities ofother “harmful algae.” As the term im-plies, this eclectic category encompassescertain true algae—primitive plants thatmake chlorophyll and carry out photo-synthesis to make their own food. Butit also includes various (usually unicel-lular) creatures, such as Pfiesteria, that

look like algae but are not plants at all.The members of this ragbag group canhurt fish when they bloom, or prolifer-ate—doing damage by producing dan-gerous levels of toxins or by other means,such as by growing so extensively thatthey rob the water of oxygen and causefish to suffocate.

Various harmful algae are infamousfor causing huge fish kills and for acute-ly poisoning animals or people who in-gest toxin-laden seafood or water. In-deed, some of Pfiesteria’s dinoflagellatecousins account for the extraordinaryred tides that have discolored and poi-soned coastal waters worldwide forthousands of years. Yet the less obviouseffects of harmful algae also need to beclarified and addressed if other seriousillnesses and death in fish—and possiblyin humans and other organisms—are tobe avoided.

Pfiesteria was first linked to the deathof fish in 1988, when tank after tank offish in brackish water at N.C.S.U.’s Col-lege of Veterinary Medicine began dy-ing mysteriously. The veterinarians no-ticed a swimming microorganism in thewater and deduced through microscopythat it was a dinoflagellate. They subse-quently noted that it became abundantin the aquarium cultures just before thefish died and seemed to disappear soonafter the fish perished. But it reappearedif live fish were added to the tanks.

Because fish from around the worldare studied at this laboratory, no one

CHESAPEAKE BAY

ALBEMARLESOUND

PAMLICOSOUND

NEUSE ESTUARY

NORTH CAROLINA

MARYLAND

Areaof detail

Area where fish killshave occurred

Region wheretoxic Pfiesteria orPfiesteria-like specieshave been found

Gulf ofMexico

TOXIC PFIESTERIA PISCICIDA (micro-graph on opposite page), sometimes alongwith a close, unnamed relative, has beenimplicated in fish kills in estuaries of NorthCarolina and Maryland (larger map). Butthese species, forming the “toxic Pfieste-ria complex,” range much farther. Mem-bers of the complex, or very similar butnot yet identified toxic microorganisms,have been found from Delaware to Al-abama’s Gulf Coast (smaller map). Thecarnage below occurred in North Caroli-na’s Pamlico Estuary in 1991 and was thefirst kill linked to Pfiesteria.

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Pfiesteria piscicida, a colorless single-celled organ-ism, can change into at least 24 distinct forms—a

rare feat.Only some are shown in the diagram (whichis actually highly simplified) and micrographs here.The creature’s shape and size depend on the type andamount of prey on the day’s menu and on environ-mental conditions. That size can range from an invisi-ble five microns (millionths of a meter) to a barely visi-ble 750 microns.

The cells become toxic in nature when fish linger intheir territory. Indeed, during the hotter seasons, thearrival of large schools of oily fish (right panel above)can trigger a “Jekyll and Hyde”personality transforma-tion. Before fish enter the scene, the cells usually existin any of three basic forms:various amorphous amoe-bae that quietly engulf algae and other prey in thebottom mud; encysted cells (also of many sizes) that

hibernate,protected by a tough outer covering;or be-nign swimming cells known as nontoxic zoospores.When the fish arrive, the nontoxic zoospores becometoxic (unlabeled arrows indicate stage changes). In addi-tion,within minutes to hours,cysts and amoebae maygive rise to nontoxic zoospores that soon become tox-ic as well. The altered zoospores send potent toxinsinto the water as they make a beeline for the fish.

The toxins drug the fish and destroy their skin, sothat disease-causing bacteria and fungi can attackmore easily as well. Meanwhile the toxic zoospores re-produce asexually and also produce gametes that fuseto form swimming, sexual products called planozy-gotes. As large sores develop on the fish,the toxic zoo-spores,planozygotes and gametes feed on substancesthat leak from the sores and on flecks of stripped skin,ingesting these materials by suction. When the fish

The Extraordinary Life

AND WATER IS BRACKISH,CALM AND COLD*(about 12 to 15 degrees Celsius)

AND WATER IS BRACKISH,CALM AND WARM†

(usually 26 degrees Celsius or higher)

Large Fillose("Star") Amoeba

Medium FilloseAmoeba

Small FilloseAmoeba

RhizopodialAmoeba

Large LoboseAmoeba

Medium LoboseAmoeba

Small LoboseAmoeba

WHEN FISH ARE PRESENT.. .

LOBOSE AMOEBA

NEW SCALY CYST

AMOEBAE

AMOEBAE

DEADFISH

Amoebaefeed on dead fish

*Findings for cold water are based on aquaculture tests.

FOOD

DEADFISH

CYSTS

NONTOXICZOOSPORES

PLANOZYGOTE

NEWLYARRIVEDFISH

NEWLYARRIVEDFISH

TOXIN

SORE

Cellsreplicate

Fish die andsink to mud

Cells feedon materialcoming from fish

Amoebae change form and feed on dead fish

Amoebae feed on dead fish

†This is the typical condition during fish kills in nature.

TOXIN

GAMETES

TOXICZOOSPORE

HURTFISH

Excrementand secretionssignal the presenceof fish

Fish die andeventually sinkto bottom

Excrementand secretionssignal the presenceof fish

Fish become ill

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Page 4: The Lurking Perils of Pfiesteria

die, many of the cells may change into amoebae, at-taching to the fish remains for a big meal.

Laboratory tests and observations from aquacul-ture facilities suggest fish can face peril in cold water,too (left panel on opposite page). Large amoebae atthe bottom of the tanks can quickly attack, kill andeat fish introduced into the system.

When dying fish disappear from the water but oth-er nutrients,such as algal prey,are abundant,the toxiczoospores and gametes often revert to nontoxic zoo-spores (left panel above). Certain cells, meanwhile,may become amoebae or hypnozygotes (a kind ofcyst). And amoebae and cysts in the bottom mudmay produce more nontoxic zoospores. In the waterthe nontoxic zoospores feed well and multiply, butthey will quickly become toxic attackers should an-other school of fish appear.

In more impoverished conditions (right panel above)the flagellated cells may opt to seek their fortune asscavenging amoebae in the mud. If the water is un-comfortably turbulent, though, swimming cells andamoebae may both turn into hibernating cysts,which are well suited for enduring adverse condi-tions. Twenty percent still survived even when wedried them for 35 days, immersed them in a concen-trated acid or base for 30 minutes or held them inbleach for an hour.

The consummate opportunist, P. piscicida even re-sorts to thievery at times (not shown). It is unable toperform photosynthesis on its own. But in a processcalled kleptochloroplastidy, zoospores often stealchloroplasts, or photosynthetic organelles, from al-gae they have eaten and use them for days or weeksto help generate energy. —J.M.B.

Cycle of Pfiesteria

AND WATER IS BRACKISH,CALM AND RICH IN OTHER FOOD(microorganisms or organic compounds from sewage or other sources)

AND WATER IS TURBULENT OR FOOD IS SCARCE

Homozygoteyst

Small Roughyst

Large Roughyst

New Scalyyst

NontoxicZoospore

ToxicZoospore

Gametes PlanozygoteFood (microbes,

dissolved organic matter,bit f d d fi h)

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FILLOSE AMOEBA

TOXIC ZOOSPORE

Drawing is not to scale

AMOEBAE

DISSOLVED NUTRIENTS

NONTOXICZOOSPORE

PLANOZYGOTE

TOXICZOOSPORE(from a recent kill)

A fewamoebaemay floatin water

Cells feed onabundant food

Cells replicate

Cells replicate

CYST

CYSTS

PLANOZYGOTE TOXIC ZOOSPORE GAMETES

GAMETESCells usually become amoebae if water is warm or become cysts if water is turbulent

Cellsreplicate

Copyright 1999 Scientific American, Inc.

Page 5: The Lurking Perils of Pfiesteria

knew where the organism had comefrom or if it was a species already knownto science. In 1989 the veterinariansasked my research group in the N.C.S.U.department of botany to help identifythe microbe and determine whether itwas responsible for the fish deaths.

The Nature of the Adversary

We soon realized that the creaturewas unique among both toxic

and nontoxic dinoflagellates in adopt-ing some forms, or stages, that do notresemble those of other dinoflagellatesat all; in those stages it looks like agroup of microorganisms called chryso-phytes. It also stood alone among thesmall subset of dinoflagellates that aretoxic. Those species (totaling about 60)produce some of the most potent poi-sons ever discovered in nature, al-though they make them for no obviouspurpose. But the newfound organismnot only appeared to poison fish—it atethem as well!

My research team learned that the ex-traordinary microbe we eventuallynamed Pfiesteria piscicida is nontoxicwhen fish are absent. When it senses fishexcrement and secretions in the water,however, it both emits toxins and swimsdirectly toward the fish materials. Thetoxins strip away the skin of the fish,damage their nervous system and vitalorgans and make them too lethargic toflee. Then the fish commonly sustain at-tacks by other destructive microbes, andbleeding sores develop where the skinhas been destroyed. With the fish unableto escape, the dinoflagellate cells feed onsloughed skin, blood and other sub-stances leaking from the sores. Later thelethal cells change from flagellated,swimming forms to more amorphousamoebae that dine on the victims’ re-

mains, sometimes becoming so engorgedthat they can no longer move.

Toxic P. piscicida can be a very effec-tive killer. In laboratory tests, toxin-con-taminated water or cultures of the cellshave killed many finfish and shellfishspecies. My research associate, HowardB. Glasgow, Jr., has found that younganimals, as well as adults of more sensi-tive species, can die minutes after expo-sure, and most victims die within hours.

We also discovered another trait thathad never been found in other toxicdinoflagellates. Remarkably, P. piscici-da can transform into at least 24 dis-tinct stages over the course of its life cy-cle. It alters its shape and size accordingto available food sources, which in-clude prey ranging from bacteria all theway up the food chain to mammaliantissue. Some of these stage changes caninvolve a more than 125-fold increasein size and can take place in less than10 minutes.

We studied Pfiesteria for two years inaquarium tanks without knowing whereit might have come from. But the infor-mation we gathered indoors prepared usfor that search. We began by looking inour own “backyard.” Every year sinceat least the mid-1980s, massive fish killshad plagued North Carolina’s Albe-marle-Pamlico Estuarine System, whichcontains the Neuse River. With helpfrom state biologists, we obtained watersamples in 1991 during a kill of aboutone million Atlantic menhaden in thePamlico Estuary.

The Adversary in Nature

When we examined the sampleswith a scanning electron micro-

scope, we saw small dinoflagellates thatlooked identical to those we had foundin the contaminated vet-school aquari-

ums. Moreover, just as had happened inour tanks, the cells seemed to disappearafter the kill ended—they were absentfrom water samples collected amongthe floating remains of fish one day af-ter the fish died. This work not onlytracked the vet-school contaminant toits probable origin but also implicatedPfiesteria as an important cause of fishdeath in nature.

What triggers toxic outbreaks ofPfiesteria? Laboratory and field experi-ments by many researchers indicatethat, among other factors, an overabun-dance of nutrients such as nitrogen andphosphorus in the water help to set thestage for these events. The shallow, slow-moving waters of many North Caroli-na estuaries are easily polluted by mate-rials from the surrounding land. Theseinclude nutrient-rich human sewage,fertilizers, certain industrial by-prod-ucts (including some rich in phosphates)and animal wastes (from many swineand poultry operations in the water-shed). When the waters become overnu-trified, algae proliferate, much as house-plants grow much better when their soilcontains added fertilizer. The abundantalgae provide a rich food source forPfiesteria, which then reproduces rapid-ly, creating legions ready to attackschools of fish should they swim intoPfiesteria-infested waters.

The estuaries of North Carolina turnout to be a very troubling place for Pfies-teria to wreak havoc. The Albemarle-Pamlico is the second largest U.S. estua-rine system outside Alaska, and it pro-vides half the area used by fish fromMaine to Florida as nursery grounds.Many young fish come to these watersto grow and develop before headingnorth or south. If such fish die in largenumbers in this crucial area, popula-tions of affected fish species up anddown the coast could eventually shrink.

Early in our research, as we estab-lished that Pfiesteria is highly lethal tofish, we also learned that fish are not itsonly victims; people can also be affect-ed. Other toxic dinoflagellates generallyhurt people by poisoning seafood. Butstudies by David P. Green of N.C.S.U.and his co-workers have found little ev-idence that Pfiesteria toxins accumulatein fish, a sign that seafood harvestedfrom Pfiesteria-contaminated watersprobably does not serve as a “middle-man” in harming human beings. In-stead the exposure route is more direct:people can become dangerously ill aftergetting toxin-laden water on their skin

46 Scientific American August 1999 The Lurking Perils of Pfiesteria

FISH KILLED DURING AN OUTBREAK OF PFIESTERIA (a term that encompasses anymember of the toxic Pfiesteria complex) often display bloody sores (left); many can also beseen to have had entire sections of their flesh eaten away (right).

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Page 6: The Lurking Perils of Pfiesteria

or after breathing the air over areaswhere fish are hurt or dying from theirown encounters with toxic Pfiesteria.

An Unwelcome Surprise

We learned about this last effect onpeople the hard way. When we

first began our investigations, we fol-lowed established safety procedures forworking with toxic dinoflagellates. Wehad been informed by specialists onother toxic dinoflagellates that in thelaboratory contact with contaminatedwater was the only danger. We did notknow that Pfiesteria produces anaerosolized neurological toxin that canseriously hurt people—the first dino-flagellate known to do so—and that wewere inhaling it.

The symptoms were so subtle at firstthat we attributed them to other causes:shortness of breath that we ascribed toasthma; problems akin to allergy at-tacks, such as itchy or mildly burningeyes or a “catching” in the throat; andheadaches and forgetfulness that we at-tributed to stress. Then one evening in1992 Howard Glasgow went to a smalllaboratory where we originally hadworked with Pfiesteria. Another depart-ment controlled the lab and had notcleaned it for some time. He found thewalls caked with evaporated, toxin-laced Pfiesteria culture. He began tryingto wipe up the mess, but after severalminutes his eyes began to burn and hegasped for breath. He lost coordination,his legs went numb and he began tovomit. He managed to crawl out of thelaboratory. We thought the extreme con-dition of the room was at fault and thathe would not have fallen ill in a well-maintained lab.

We refused to use that laboratoryagain and had new facilities construct-ed. These were supposed to have beencarefully ventilated, but unknown to us,the contractors mistakenly vented theair from the toxic-culture lab directlyinto Howard’s office. Over the next fewmonths, this normally cheerful, detailedscientist became extremely moody andsometimes seemed disoriented and un-able to focus on even simple tasks. Thishighly intelligent man, with a razor-sharp memory, suddenly could not re-call conversations from earlier in theday. Finally, after a period of intensivelab work, even his long-term memorysuffered. He could not find his wayhome, remember his phone number oreven read, and he struggled to speak.

After two months away, he recoveredand returned to work. But over the nexttwo years, strenuous exercise caused re-lapses of aching joints, burning musclesand bouts of disorientation.

Before we realized that Pfiesteria canproduce aerosolized toxin, 12 peoplefrom four different labs were sickenedfrom toxic cultures. Three of us, myselfincluded, have sustained some persis-tent problems we did not have before webegan to study toxic Pfiesteria. In thepast six years I have had chronic bron-chial infections and 16 bouts of pneu-monia; to cope with the infections, I takeantibiotics for about a third of each year.

We now conduct our research in aspecially designed biohazard III facility,using more precautions than are neededfor most research with the AIDS virus.The lab is fitted with air locks, deconta-mination chambers and other safety fea-tures, and researchers wear full hoodedrespirators supplied with purified air.

Chronic Effects in the Field

People exposed to toxic Pfiesteria out-breaks in nature have reported simi-

lar symptoms. Divers, fishermen andothers working in contaminated waterswhile fish were showing signs of Pfieste-

The Lurking Perils of Pfiesteria Scientific American August 1999 47

Fish become sluggishor disoriented, or both

Feeding becomes depressed;reproduction declines;

death rates of newbornsand the young increase

Fish become morevulnerable to predators

Tumors and other chronic diseases may develop

Survivors become prone toinfections and other disorders

Critical habitatsbecome severely

damaged

Fish that do not die become stressed

Sublethal levels of toxinspromote immune system

suppression in surviving fish

Toxins damageeggs and young fishdirectly; death rates

of newborns and the young increase

Toxins pass upthrough carnivores

in the food chain andaccumulate in them

Harmful algae crowdout other species androb water of oxygen

Algal blooms occur(cells proliferate extensively)

Outbreaks of toxin-producingspecies (such as Pfiesteria) occur

Fish population declines

BEYOND KILLING MANY FISH AT ONCE, harmful algae can hurt fish in otherways. In the long run, these less obvious effects might lead to more persistent declinesin fish populations than are caused by dramatic fish kills. The term “harmful algae” isa loose, eclectic category encompassing noxious algae as well as several species, such asPfiesteria, that are more animallike than plantlike.

How Harmful Algae May Cause Chronic Declines in Fish Populations

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ria poisoning have described respiratoryproblems, headaches, extreme moodswings, aching joints and muscles, dis-orientation, and memory loss. Suchanecdotal reports have recently beenbolstered by formal clinical assessments.

In 1997, for example, three smalloutbreaks of Pfiesteria led Maryland’sgovernor to close the affected waters inChesapeake Bay for several weeks. Re-ports of strange symptoms in peoplewho had been in the affected areasprompted the Maryland Department ofHealth and Mental Hygiene to organizea medical team to investigate. Amongthose who complained were heavily ex-posed fishermen—who described get-ting lost on a bay they had workedtheir entire lives or losing their sense ofbalance and concentration. Throughneuropsychological testing, a medicalteam led by J. Glenn Morris, Jr., of theUniversity of Maryland School of Med-icine documented “profound” learningdisabilities in the patients. The severity

of their cognitive dysfunction was di-rectly related to their degree of expo-sure, and the patients recovered theirfaculties over the next few months.

Doctors have difficulty diagnosingthis “Pfiesteria syndrome” conclusively,however, because the specific toxins atfault have not yet been identified (as isthe case with many toxic algae). With-out that information, investigators can-not examine how the chemical acts inthe human body, nor can tests be de-signed that definitively identify it in theblood or tissues. Fortunately, progressis being made. Peter D. R. Moeller andJohn S. Ramsdell of the National OceanService in Charleston, S.C., have semi-purified components of Pfiesteria tox-

ins that destroy fish skin and affect thenervous system in rats (which are stud-ied as a model for humans).

Our own lingering health problemshave led us to devote much attention tothe possibility that Pfiesteria mightcause chronic effects in fish that sustainnonlethal exposures. In lab experi-ments, we subjected fish to low concen-trations of toxic Pfiesteria and moni-tored the animals for up to three weeks.The fish appeared to be drugged, andthey developed skin lesions and infec-tions. Tests revealed that white bloodcell counts were 20 to 40 percent belownormal levels, suggesting that Pfiesteriatoxins may compromise the function-ing of the immune system and makefish more susceptible to disease. Autop-sies of fish that were affected have re-vealed damage to the brain, liver, pan-creas and kidneys.

Weakened immunity, increased dis-ease and periodic fish kills can all con-tribute to a decline in fish stocks. But

other problems couldseriously affect theability of fish popula-tions to recover. Re-search has shown thatwhen toxic Pfiesteria isin the water, the eggsof striped bass and oth-er commercially valu-able fish fail to hatch.Experiments by San-dra E. Shumway ofSouthampton Collegeand my graduate re-search assistant JeffreyJ. Springer have estab-lished that Pfiesteriaalso kills shellfish lar-vae, sometimes withinseconds of contact,

and causes young bay scallops to losetheir ability to close their shells. In thatcondition, they would be highly vulner-able to predators.

The Bigger Picture

As we became increasingly concernedthat Pfiesteria could threaten the vi-

ability of fish populations, we began towonder whether this phenomenon waspart of a broader trend. Dogma hadlong held that most finfish and shellfishexposed to sublethal doses of toxinsfrom harmful algae suffer no ill effects.But could many harmful algae causetrouble that had been overlooked—per-haps by interfering with reproduction,

with the survival of sensitive young fishor with resistance to disease? We alsowondered whether there was evidencethat these organisms could producesustained or subtle health problems inpeople.

Few researchers have explored thesequestions or looked intently at the long-range effects of harmful algal blooms onthe ecosystem as a whole. Nevertheless,a cluster of findings indicates cause forconcern. These findings become espe-cially disturbing when we note that as agroup harmful algae are thriving. Someexperts have pointed out that within thepast 15 years, outbreaks of certain harm-ful algae seem to have increased in fre-quency, geographic range and virulencein many parts of the world.

Consider these examples. When bayscallops were exposed to small amountsof toxin from the dinoflagellate Alexan-drium tamarense, their gut lining waseaten away, and their heart rate andbreathing slowed. Other dinoflagellatesproduce ciguatera toxins that can accu-mulate in reef fish without killing themoutright. The fish can grow largeenough to be harvested as food for peo-ple, who then become sick. In fact,more human illness is caused by cigua-tera-laden barracuda, red snapper,grouper and other tropical fish than byany other seafood poisoning. The symp-toms can relapse for years, often trig-gered by alcohol consumption. Cigua-tera toxins can also interfere with thenormal function of white blood cellscalled T lymphocytes and thereby com-promise the immune system. Recentwork suggests that these toxins maytake a similar toll on fish, resulting inimpaired equilibrium, fungal infectionsand hemorrhaging.

Two types of cancer, disseminated neo-plasia (similar to leukemia) and germino-mas (which attack the reproductive or-gans), affect such shellfish as blue musselsand soft-shell clams. Studies have linkedthese cancers to certain dinoflagellatesthat produce saxitoxins, the same toxinsthat can cause sometimes fatal poisoningin people who eat contaminated shell-fish. People who recover from acute sax-itoxin poisoning may relapse with malar-ialike symptoms for years afterward. In-gestion of shellfish tainted with okadaicacid from toxic dinoflagellates along Eu-ropean coasts normally causes people tohave diarrhea, but smaller, chronic doseshave caused tumors in lab rats and hu-man tissues. Okadaic acid can also de-stroy cells in the hippocampus of the

48 Scientific American August 1999 The Lurking Perils of Pfiesteria

RESPONSE OF BAY SCALLOPS to Pfiesteria in the laboratoryis one of several indications that it can endanger the long-termhealth of fish it does not kill. When healthy scallops, such as theone on the left, were exposed to sublethal densities of toxic cells,they became unable to close their shells (right), a disability thatwould increase susceptibility to predation in the wild.

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brain, an area important in memory, andcan lead to suppression of the humanimmune system.

Chronic health problems from harm-ful algae are not restricted to marineenvironments. Blooms of blue-green al-gae (cyanobacteria) can take most ofthe oxygen from the water at night, sothat fish become stressed and weakenedand more vulnerable to disease. More-over, toxins from these algae have causedliver, lung and abdominal tumors inmice, as well as mild to severe liverdamage in humans.

Fish as Canaries

To combat the unwanted effects ofharmful algae, scientists must first

“know the enemy” more thoroughly.Many harmful algae are so poorly un-derstood that even fundamental factsabout their life cycles remain unknown.Scientists must also chemically charac-terize more of their toxins, so that im-proved warning systems can be devel-oped for determining when waters areunsafe.

Armed with that information, inves-tigators will be able to assess how thetoxins are processed in the human bodyand whether they are stored in our tis-sues. We will also be able to make prog-ress in answering other important ques-tions, such as: What is the range of acuteand chronic effects of the toxins on thehuman nervous and immune systems,and how long do these effects last? Whatare the overall consequences to fishhealth? How do the toxins interact withother microorganisms and with pollut-ants to hurt fish, wildlife and humans?

For many species of harmful algae,the factors that stimulate increased ac-tivity are as incompletely understood asthe organisms’ life cycles. Clearly, nutri-

ent pollution has stimulated the growthof Pfiesteria and certain other membersof the group. Some ecologists believethat nutrient overenrichment and othertypes of pollution have contributed to aserious general imbalance in manyaquatic ecosystems. Large algal bloomsand toxic outbreaks, they assert, aresymptomatic of this imbalance as wellas participants in its perpetuation.

This ecological breakdown may havemany causes. Continuing losses of thewetlands that act as the earth’s kidneyshamper the ability of waterways tocleanse themselves. Some algal bloomshave coincided with El Niño events,suggesting that warming trends in glob-al climate may stimulate the growth ofthese species and extend their range.These climatic changes also createflooding that washes additional nutri-ents and other pollution into rivers andestuaries. Further, inadequate environ-mental regulations are providing toolittle protection for our waters at a timewhen nearly two thirds of Americans

live within 50 miles of a coastline.There are more people on the earththan ever before. They are using rela-tively scarce freshwater supplies at anever increasing rate, while they are alsogenerating more and more wastes thatdegrade both fresh and marine waters.

As we pulled anchor during the Oc-tober 1995 fish kill, many thoughtswere in my mind. I was keenly awarethat Pfiesteria is but one type of harm-ful microorganism that can disruptboth fish resources and human health.Ultimately, water quality, human healthand fish health are strongly linked. Allof us—scientists, politicians, resourcemanagers, fishermen and other cit-izens—need to work together to learnmuch more about the chronic as well asthe acute effects of harmful algae. Wemust also become more proactive in ad-dressing the state of our waterways, in-stead of reacting to each fish kill as if itwere a limited, isolated crisis. In protect-ing vulnerable fish, the health we sparemay also be our own.

The Lurking Perils of Pfiesteria Scientific American August 1999 49

The Author

JOANN M. BURKHOLDER, the world’sforemost authority on Pfiesteria, is professor ofbotany and a Pew Fellow at North CarolinaState University. She has received many awardsfor her research and her contributions to envi-ronmental policy and education, including theConservation Achievement Award in Sciencefrom the National Wildlife Federation, the Ad-miral of the Chesapeake Award, and the Scien-tific Freedom and Responsibility Award fromthe American Association for the Advancementof Science. She can be reached via e-mail [email protected]

Further Reading

New “Phantom” Dinoflagellate Is the Causative Agent of Major Estuarine

Fish Kills. J. M. Burkholder, E. J. Noga, C. W. Hobbs and H. B. Glasgow, Jr., in Na-ture, Vol. 358, pages 407–410; July 30, 1992.

Neoplasia and Biotoxins in Bivalves: Is There a Connection? Jan Landsberg inJournal of Shellfish Research, Vol. 15, No. 2, pages 203–230; June 1996.

Implications of Harmful Microalgae and Heterotrophic Dinoflagellates in

Management of Sustainable Marine Fisheries. JoAnn M. Burkholder in EcologicalApplications, Vol. 8, No. 1 (Supplement), pages 537–562; February 1998.

Marine Ecosystems: Emerging Diseases and Indicators of Change. Paul Epsteinet al. Year of the Ocean Special Report. Center for Health and the Global Environ-ment, Harvard Medical School, Boston, 1998.

The Aquatic Botany Laboratory at North Carolina State University site on the toxic Pfieste-ria complex is available at www.pfiesteria.org on the World Wide Web.

HIGHLY PROTECTIVE EQUIPMENT is now de rigueur for researchers studying Pfieste-ria and its close relatives. People can be harmed not only by having contaminated watertouch their skin but also by inhaling Pfiesteria toxins from the air.

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