Protecting Ourselves from Shellfish Poisoning

Feature Articles Protecting Ourselves from Shellfish Poisoning Molecular probes deployed by California scientists are just the latest weapons in our species long battle with harmful algae Mary Wilcox Silver As the sun set over San Francisco Bay on July 15, 1927, area residents had plenty to talk about: Aviators Ernie Smith and Emory Bronte had just become the first to fly a single-engine aircraft, City of Oakland, 2,100 miles nonstop from Oakland to Hawaii. But the next day, a panic began to grip the area. Residents who had eaten mussels gathered along the beaches around San Francisco were falling gravely ill. That day the San Francisco Examiner reported the first two deaths on its front page. An alarm went out. Signs were posted along the beaches, and scientists and public-health officials got to work to understand what was happening. Thanks to the research that followed the San Francisco scare, shellfish poisoning is now rare in California. Indeed, a monitoring strategy developed in the state in response to the incident has saved countless lives around the world over the past eight decades. Scientists have learned a great deal about what can make shellfish and other Mary Wilcox Silver, a native of San Francisco, is a professor in the Ocean Sciences Department at the University of California, Santa Cruz. She has mostly worked on the microbial communities that live on floating marine snow and studied how these ubiquitous particles transport materials into the ocean s deep interior. In the past decade she also has become interested in the role of toxic microalgae in coastal oceans, and especially how the toxins may be permeating marine ecosystems, affecting animals living both in the water and on the seafloor. This article is adapted from the Winter 2006 Synergy Lecture at UCSC. Address: Ocean Sciences Department, University of California, Santa Cruz, CA 95064. Internet: msilver@ucsc.edu aquatic organisms dangerous to eat, and this knowledge has been put to practical use in harvesting regulations, monitoring and food-testing programs and public education. At the same time, we ve also learned that people have been protecting themselves from ingesting marine toxins for millennia and perhaps much longer. Today, even as modern technology is being harnessed to tackle this daunting and persistent problem, we find that ways of protecting ourselves from toxins in seafood likely have been a part of maritime cultures for thousands of years of human history and may even have roots in prehistoric culture. Shellfish and Ancient Diets What was happening on the beaches of San Francisco that warm July day, then, was anything but new. People living around the Pacific Ocean have always eaten shellfish, and consuming these filter-feeders has probably always posed certain risks. The San Francisco scare was one of the occasions that expanded our understanding of those risks. Shellfish are easily harvested from shallow aquatic environments in much of the world, where they are proteinrich food for predators, including people. It is not surprising that evidence of their use is found throughout the archaeological record left in Africa by earlier hominids, Homo erectus and H. habilis, and by modern human beings. Along the waterways of the world s continents can be found the remains of shell mounds that, in association with the artifacts found with them, have led anthropologists to speculate that hominids ate shellfish, including mussels and other bivalve mollusks, possibly as early as one million years ago. Anatomically modern H. sapiens left sizable middens on coastal sites in Africa and at various locations in Eurasia, supplying good evidence that shellfish were collected more than 100,000 years ago. The middens found up and down the West Coast of North America are much younger, mostly less than 10,000 years old. Between the new and ancient middens, our record of coastal dietary culture thins out, owing to the fact that the world s sea level rose and fell multiple times during ice ages. Our ancestors would have moved out onto continental shelves to collect fish during cooler periods, leaving behind evidence that is underwater today. Underwater archaeology has located some of these sites, but wave disturbance and wave action have destroyed much of the record. About 10,000 years ago, sea-level rise slowed, so that coastal archaeologists have a good record of shellfish use in locations such as the islands off southern California. Was eating shellfish risky in ancient times? There is intriguing evidence that it was. Consider, from the Jewish tradition, the laws of kosher eating set out in the book of Leviticus (here, the King James Bible version): These shall ye eat of all that are in the waters: whatsoever hath fins and scales in the waters, in the seas, and in the rivers, them shall ye eat. Whatsoever hath no fins nor scales in the waters, that shall be an abomination unto you. 316 American Scientist, Volume 94

McCormick Library of Special Collections, Northwestern University Library Figure 1. Mussels are a traditional food of many of the indigenous peoples of the Pacific coast of North America including the Quileutes, whose culture was documented in the photographs published by Edward S. Curtis in the early 20th century. Curtis photographed this Quileute mussel gatherer in 1900. Certain coastal peoples have long avoided harvesting shellfish during warm seasons or when bioluminescence was observed in ocean waters strategies that predate modern protections against the algal toxins that can be ingested with fish and shellfish. Today the Quileutes are collaborating with scientists on new monitoring tools, while other scientists and engineers are employing technology to keep better watch on harmful marine algae. In the views of the rabbis who dictated the Kashrut, filter-feeding shellfish, crustaceans, gastropods and cephalopods were scavengers, indiscriminate eaters, unclean animals. References to avoiding shellfish can also be found in certain Islamic and Christian traditions. Although other explanations have been offered, knowledge of the special hazards of eating shellfish might have informed the makers of these laws. The traditions of the indigenous peoples of the Pacific Coast of North America also hint at ancient knowledge of shellfish dangers. Anthropologists have found that some of these tribes customarily watch for the ripening of elderberries, a sign of summer, as a signal that it is time to stop harvesting shellfish. And sentinels were traditionally posted on cliffs in the Pacific Northwest to watch the sea for bioluminescence an indicator, we now know, of a particularly dense bloom that might make shellfish dangerous to eat. Today scientists and physicians are working with the Quileute Tribe in the Olympic region in a collaboration intended both to develop new monitoring tools to protect human health and to learn about the effect of long-term exposure to shellfish toxins. To understand these intriguing connections between human culture and shellfish poisoning, it is useful to take a close look at the biology behind shellfish poisoning. Toxins in the Marine Food Web As the ancient rabbis recognized, a mussel will consume just about anything. As collectors of tiny particles floating in the water, the bivalves, cemented to the seafloor, continuously siphon great volumes of water, straining out diatoms and other nutritious tidbits. A mussel harvested on any given day will contain whatever was in the water around it that day, sometimes along with traces of items it s picked up on other days. These can include viruses, bacteria, pollutants, parasites www.americanscientist.org 2006 July August 317

University of California. Berkeley Library Figure 2. San Francisco s seafood-poisoning scare struck in 1927, competing for prominence in the Examiner with the arrival of a beauty queen and the disappearance of a husband. Before this incident, the known hazards from shellfish were diseases (now recognized as bacterial and viral) attributed to water contamination. But researchers at the Hooper Foundation in San Francisco and the University of California, Berkeley, ultimately identified a naturally occurring alga as the culprit and devised a method for monitoring shellfish for the presence of a neurotoxin produced by the alga. and toxic algae. Even if these don t affect the mussel, they can spell trouble for a susceptible animal that eats it. Viruses and bacteria are perhaps the best-known risks associated with eating shellfish. These risks grew in Europe during medieval times as settlements around estuaries and bays grew larger, polluting the enclosed waters with coliform bacteria from human waste. Salmonella bacteria including S. typhii, the cause of typhoid fever, began to be found in shellfish with regularity. In the Middle Ages, shellfish were also implicated in cholera outbreaks, since they can harbor Vibrio species including V. cholerae. Fortunately bacteria and viruses such as hepatitis A and poliovirus can be destroyed by cooking, and so measures to prevent shellfish-borne disease have included cooking practices along with closings of contaminated areas during disease outbreaks. Before the San Francisco scare, new immigrants along the California coast were unaware of the dangers of eating shellfish, either cooked or raw dangers known to some of the native inhabitants of the region. But in 1927 San Francisco beachgoers learned that even cooked shellfish from a clean environment could sicken and kill. The reason is that the organisms I study certain of the tiny unicellular marine organisms known as dinoflagellates and diatoms produce potent toxins, poisons that are not destroyed even by cooking. Mollusks feeding on these toxic algae are generally thought to be unaffected by these substances, but the toxin acquired through filtering its food may, like the other shellfish contaminants mentioned above, be enough to kill a susceptible predator that eats the mussel. Recent research has shown that knowledge of the effects of these toxins exists in many aboriginal cultures. But the San Francisco incident came as a surprise to an urbanizing nation that knew only of the shellfish hazards associated with pathogens. Even after newspaper warnings were issued and signs posted on the beaches, some people continued to eat mussels. The worst affected were those who ate large numbers of mussels on an empty stomach, feasting on these especially tasty mollusks on a warm summer s weekend with a good low tide that allowed easy access to the mussel beds. The neurological effects set in soon, usually within an hour or so. Ultimate- 318 American Scientist, Volume 94

ly more than 100 people were affected, and a handful died. Discovering paralytic shellfish poisoning or PSP, as this syndrome is now known, took some work. Scientists first suspected backwash from local sewage, materials leaking from garbage barges, or even copper from a disintegrating tanker. But three men physicianscientists Herman Sommer and Karl Meyer of the Hooper Foundation (later part of the University of California, San Francisco) and Charles Kofoid, a microbiologist at UC Berkeley pursued the case further as the early leads appeared inadequate and the geographic extent of the poisoning became known. They began to look closely at water samples taken on San Francisco s open coast and speculated that there might be something of natural origin making the water itself toxic. After several more years of study, more cases of shellfish poisoning in the region and elegant scientific detective work, Sommer, Meyer and Kofoid began to focus on a microorganism a photosynthetic swimming alga, a dinoflagellate and came up with their prime suspect. They turned out to be right: An organism we now call Alexandrium catanella was the culprit revealed in an article published in 1937. This was the first time that a waterborne alga was found to be responsible for shellfish poisoning. The substance produced by A. catanella, which sometimes can cause a luminescent red tide when the cells become especially abundant, was first synthesized in 1977. Saxitoxin is tasteless, odorless and water-soluble, with a toxicity similar to that of the biological-weapon poison ricin. When you eat a mussel containing saxitoxin, you may first experience tingling in your fingers, lips, face and extremities as if someone is poking you with pins. Then your lips go numb, along with your arms, legs and neck. It s time to get to the doctor! You re in the first stages of paralysis, and without medical assistance you may die, because you will be unable to breathe. There is no antidote, and just a few milligrams can kill you. Patients survive with help from intravenous fluids and a respirator. The algal cells capable of wreaking this havoc are almost spherical and about 40 micrometers long; that is, a Figure 3. Alexandrium catanella (as it is now called) was identified in 1937 as the cause of the 1927 San Francisco shellfish-poisoning incident. It is a colony-forming, swimming alga that produces a neurotoxic substance called saxitoxin. Filter-feeding mollusks such as mussels take in the algal cells and frequently appear unaffected by the toxin (though those that are affected and look unhealthy are usually not harvested); however, a person eating a healthy-looking mussel that contains saxitoxin can die from respiratory paralysis. The same reddish alga is capable of producing a toxic red tide when cells become very abundant. In many cases, discolorations of the sea are produced by nontoxic algae. The name red tide is often used colloquially to suggest harmful concentrations of algae, including ones that have toxins. (Image courtesy of the author.) Woods Hole Oceanographic Institution Figure 4. Algal toxins are one of an array of potential hazards associated with eating shellfish. Most dangers come from biological and chemical contamination of the water that bivalve mollusks continuously siphon as they feed. And many contaminants can be destroyed by cooking. Decades of monitoring of shellfish safety in California have led to the routine closing of harvesting areas during warm months. Commercial shellfish growers protect their beds from contamination and are required to monitor their products for contamination. It is common in US coastal towns such as Bourne Bay on Massachusetts s Cape Cod (above) to find areas closed to recreational harvesting when contamination is detected or during seasons when water conditions are conducive to harmful algal growth. www.americanscientist.org 2006 July August 319

Jeff Poklen, Santa Cruz, Calif. Figure 5. Bizarre symptoms and deaths among marine animals alerted California biologists to the appearance of a toxin previously unknown in the state, one that causes amnesic shellfish poisoning in human beings. It turned out that anchovies (lower left) were feeding on planktonic (floating) algae, Pseudo-nitzschia, that produced a neurotoxin called domoic acid. The cells and their toxin were concentrated in the anchovies digestive tracts and then taken up by pelicans feeding on schools of anchovies around Monterey Bay. Domoic acid was first identified in a seaweed, Chondria armata, that washes up on beaches in Japan (top, middle), and was later found in the unrelated Pseudo-nitzschia (top right). Domoic acid killed several people who ate a crop of farmed mussels from Prince Edward Island in 1987 that had been contaminated by toxic Pseudo-nitzschia. The toxin has also been found in high concentrations, along with fragments of toxic Pseudo-nitzschia, in the feces of humpback whales. (Photographs courtesy of the author (Pseudo-nitzschia); National Undersea Research Program (anchovies); University of California, Berkeley, Herbarium (Chondria); Chad King/MBNMS (whale)). Figure 6. Paralytic and amnesic shellfish poisoning (PSP and ASP) share many symptoms. PSP is more likely to be fatal, causing death from respiratory paralysis. The cause of ASP, domoic acid, is an amino acid that attacks some types of nerve cells, especially those in the hippocampal memory centers in the brain; although it is less likely to cause death, the damage can be long-lasting. line of about 25 would be a millimeter long. The reddish cells form colonies, an important fact because they thus become food for organisms that cannot capture smaller particles. Since the discovery of PSP, A. catanella and saxitoxin (also known as STX) have turned up in other contexts. Hong Kong s harbor has been known to turn red; indeed, toxic algal events have been observed along the mid- and upper-latitude coasts of every continent except Antarctica. And pilots who flew U-2 spy missions over the Soviet Union were given tiny pellets of saxitoxin extracted from the algae and reportedly were instructed to take the suicide capsules if they were shot down. The Pelican Peril In 1991, a new kind of incident in California caught the monitoring community by surprise. Fortunately for the 320 American Scientist, Volume 94

Figure 7. Sea lions are among the animals most affected by the amnesic shellfish poisoning toxin. The Marine Mammal Center in Sausalito, California, rescues sea lions that are seen onshore exhibiting the toxin s symptoms such as seizures, head-weaving and lethargy. Several dozen such strandings took place during the spring of 2006. The animals can be treated with anticonvulsant agents and hydration. (Photograph courtesy of the Marine Mammal Center.) state s human population, birds and marine mammals served as sentinels in this case. This may be the only case in which the local presence of a poisonous alga was first recognized because of animal deaths. To Californians familiar with PSP, it was soon clear that a different poison was now at work. This time, brown pelicans and cormorants began washing ashore in the Monterey Bay area. Not all the birds were dead, and the survivors exhibited very odd behavior. Working with veterinarians, we biologists proceeded to examine their stomach contents and found anchovies full of a different algal species: a common coastal diatom now known as Pseudonitzschia. These slender cells are about one-tenth of a millimeter long, over twice the length of A. catanella, and they also form long chains. As we studied what was known about this organism, we realized that our local species had long been misidentified in the region, so we had to use a newly revised taxonomy of the Pseudo-nitzschia genus. It turns out that within this genus are species that are poisonous in some places and not poisonous in others, along with species that are mostly or rarely poisonous. The poisonous species which today can be distinguished using electron microscopy or molecular tools make a neurotoxin quite different from saxitoxin, one called domoic acid. This is a naturally occurring amino acid that affects glutamate receptors in the brain and particularly damages memory centers. Our waters in Monterey Bay contained two toxic and a number of nontoxic species of Pseudo-nitzschia. The pelicans and cormorants behavior was a manifestation of a toxin that causes amnesic shellfish poisoning in humans. The phenomenon acquired this name from an earlier incident, this one involving people who ate a crop of farmed mussels from Prince Edward Island, on Canada s east coast, in 1987. The victims suffered gastrointestinal symptoms and terrible headaches, but also hallucinations, seizures and memory loss; several died. In the Canadian event, the source of the toxin was Pseudo-nitzschia, a toxin that strangely turned out to be an anti-worming agent, previously known in Japan, as I ll describe below. How had the birds come down with domoic acid poisoning? One lesson clearly demonstrated by the 1991 incident is that animals other than shellfish can be poisonous. Pelicans and cormorants forage on schooling fish anchovies in particular. Off the California coast, schools of anchovies appear as large shadows on the sea surface. A brown pelican in search of a meal dives into a school and scoops up a fish in its expandable pouch. For their part, anchovies acquire food with the aid of gill rakers, comblike structures that allow them to sieve from the water microorganisms of millimeter size. The anchovy concentrates this food in its stomach. Algae thus end up in an anchovy s digestive tract, which can be a condensed packet of partially digested toxic cells. But the fish itself is normally unaffected by the domoic acid and typically contains little toxin in its tissue. When a pelican dives and scoops up an anchovy in its pouch, it gets the fish s stomach contents as well. Fish like anchovies and sardines turn out to be responsible for many of the poisonings of marine vertebrates in our area. Since the 1991 incident we ve found evidence that a great variety of organisms are affected by domoic acid in the marine food web. We ve found domoic acid and the tiny skeletons of Pseudonitzschia in the feces of humpback whales, in mole crabs and fish such as white croakers, a favorite of pieranglers. My UC Santa Cruz colleagues Sibel Bargu and Kathi Lefebvre examined the feces of the largest mammal on Earth, the blue whale, and found fragments of the toxic species Pseudonitzschia australis along with concentrations of domoic acid that were 10 times the level considered dangerous to humans. In the case of the blue whale, neither shellfish nor anchovies are the source; the domoic acid is being passed along by krill, the whale s chief food source. Figure 8. Domoic acid has been studied as a possible cause of marine-mammal strandings. Domoic-acid levels and concentrations of Pseudo-nitzschia cells have been monitored along the California coast since 1998 and compared with stranding data. Although an initial data set showed a correlation, the effect is less clear in recent data. Recent sampling shows, however, that the Pseudo-nitzschia cells found near the shore are generally less toxic than those offshore in locations where sea lions are known to forage. www.americanscientist.org 2006 July August 321

And among the animals most obviously affected are sea lions. This year stranded sea lions are turning up on California beaches along with disoriented pelicans. Sea lions have indeed become the sentinels of the central California coast. Rescuers from the Marine Mammal Center at Sausalito look for animals exhibiting seizures, headweaving, strange arching postures, lethargy and unresponsiveness. They restrain the animals and transport them to rehabilitation centers, where their symptoms can be treated with anticonvulsant agents and hydration. Is domoic acid, in fact, to blame for the strandings of marine mammals that are becoming so frequent in California? It turns out that the connection is becoming less clear the more data we get. Frank Lane Pictures/Photo Researchers, Inc. Figure 9. Mouse units were established as the measurement of shellfish toxicity more than 70 years ago and remain the international standard today. The team of investigators assembled in 1927 to find a way to prevent a repeat of the San Francisco incident initially did not know the cause of the shellfish poisoning, but they quickly developed a method for measuring the toxicity of shellfish. A liquid extract taken from ground-up mussels (top left) is injected into a 20-gram white mouse; its effect on the animal is a reliable indicator of whether the mussel is safe to eat. The graph above, published in 1937 in the Journal of Pathology, established the connection between the the mouse bioassay (line A, showing mouse units of toxin), the concentration of all dinoflagellates (line B) and the prime dinoflagellate suspect (the species now called Alexandrium catanella, line C) in San Francisco waters over the years 1932 35 (Sommer et al. 1937). These results demonstrated that A. catanella was the source of paralytic shellfish poisoning. (Mussel photograph courtesy of the author.) In 1998, Christopher Scholin and his colleagues at the Monterey Bay Aquarium Research Institute (MBARI) began taking measurements of the abundance of Pseudo-nitzschia cells in the bay s waters and studied how they correlated with marine-mammal strandings observed by Frances Gulland of the Marine Mammal Center. During their initial study period, the correlation appeared strong and positive, but as I ve added data over the following years, the apparent correlation has become muddied. The links between blooms of toxic Pseudo-nitzschia and strandings of sea lions that show symptoms of domoic acid poisoning are not clear. We are beginning to notice, however, that the diatom cells seem to be more toxic offshore than close to shore, where we monitor the algae. The more-toxic offshore populations, unfortunately, are located in the sea lions foraging range, and thus we may be underestimating their exposure in more dangerous waters than those we monitor close to shore. Domoic acid was synthesized by chemists in 1982, well before it was known to occur in phytoplankton. It was first isolated in Japan in 1953, not from a diatom but from Chondria, a red seaweed on the Japanese coast. It turns out that the toxin has been known for a very long time in Japan, where in small amounts it has a traditional use in the home. Chondria is known to kill flies that settle on the seaweed; this evident toxicity has been put to long use by Japanese parents as an antihelminth, a treatment for internal parasites in children. But What to Do? I ve left out what may be the most important part of the story of shellfish (and anchovy) poisoning: how people have responded to this hazard in our natural environment and managed to keep it largely at bay. Ever since the San Francisco incident, science has played a major part in protecting us from shellfish poisoning, a battle in which we re now deploying 21st-century tools. For the most part, though, we continue to rely chiefly on a 20th-century tool: the mouse. When the Berkeley and Hooper Foundation investigators discovered what had killed the people of San Mateo and San Francisco in 1927, they set to work developing a way to prevent future deaths. They developed a monitoring technique that still is, remarkably, in widespread global use today. The concept is fairly simple. Mussel tissue is ground up, and the toxins extracted using an acidic agent. After filtering, the liquid phase is injected into a mouse. A low concentration of toxin may have little effect; a high concentration will kill the mouse quickly. Thus the toxicity of shellfish is routinely measured in mouse units, an indication of how quickly it kills a 20-gram white mouse. This bioassay, the very test that proved that a waterborne alga was the culprit in the San Francisco poisonings and that was first used in 1927, remains the international gold standard for detecting PSP. The impressive field observations and clever laboratory work of Sommer and his Hooper Foundation colleague W. Forest Whedon in the 1930s gave us the convincing evidence 322 American Scientist, Volume 94

Figure 10. Paralytic and amnesic shellfish poisoning have now been reported in the mid-latitude coastal regions of all the inhabited continents. Dots show reported blooms of toxic algae (distinguished by the types of poisoning associated with them) between 1970 and 2005, as compiled by the U.S. National Office for Harmful Algal Blooms at the Woods Hole Oceanographic Institution. Ciguatera fish poisoning is a third hazard seen commonly in the tropics; it is caused by eating reef-visiting fish that have consumed ciguatoxin-producing dinoflagellates, which typically live on seaweeds or on damaged corals. (Data from WHOI.) that the abundance of Alexandrium catanella cells correlates well with mouse units of PSP toxicity. As a result, California and now other states and countries around the world have monitoring programs and are able to prevent deaths by closing shellfishing beds when there is a dangerous increase in toxicity. Commercial shellfish growers do their own testing before preparing their harvest. Because the monitoring was able to show seasonal patterns of toxicity, California could set a seasonal quarantine, routinely forbidding sport harvesting of shellfish during late spring, summer and early fall. Scientists would like to find a more rapid, direct and real-time way to monitor hazards from harmful algal blooms, and a way that would not require sacrificing animals. MBARI s Scholin and his team of engineers and scientists have developed a way to do this, without ever leaving their offices. Basically they have designed and constructed a robotic undersea lab to do the job. Scholin began by developing DNA probes that recognized the various local species of toxic Pseudo-nitzschia. His method broke apart cells vacuumed onto a filter, and then he exposed the cell material to the gene probes that recognize the species of interest. Scholin s team developed the Environmental Sample Processor (ESP), a seagoing lab that is modular and programmable and can test for the presence of a wide array of microorganisms, Figure 11. Monterey Bay is the site of efforts to develop, test and deploy automated technology to continually monitor hazards from toxic algae. Scientists at the Monterey Bay Aquarium Research Institute (MBARI) and the National Oceanic and Atmospheric Administration have developed sensors for algal toxins and DNA probes that recognize harmful local algal species. Collaborating engineers have helped build a seagoing laboratory that samples and tests the bay s waters, providing real-time monitoring data. Monterey s sea lions, which are frequently affected by the toxins, find additional uses for MBARI s moorings. The unit shown here collects various kinds of oceanographic data. (Photograph courtesy of MBARI.) www.americanscientist.org 2006 July August 323

Figure 12. On Tanzania s Zanzibar Islands, a night s fishing comes to a climax as fishermen haul their catch in from dhows in the morning and present it to fishmongers in a lively onshore auction. During her sabbatical research, the author and a translator talked with Zanzibar fishermen after they unloaded their catch, conducting interviews to learn whether ciguatera fish poisoning (CFP) was a problem in the area. She learned why the area s residents do not consider CFP a problem: They avoid eating the livers of fish species producing symptoms recognized in western medicine as CFP, the liver being the organ where the poison concentrates, even though livers of other fish are much prized in the islands. Such an avoidance pattern is shown by people everywhere who avoid eating the poisonous parts of land plants. (Photograph courtesy of the author.) as well as the toxic algae. Greg Doucette from the Charleston laboratories of the National Oceanic and Atmospheric Administration developed new sensors for the algal toxins, ones that Scholin could add as a module to the ESP. The robot is now in the testing stage in Monterey Bay, where it is showing its Figure 13. Bioluminescence, frequently observed in offshore waters, is sometimes an indication of harmful algae in the water a light show observed when toxin-producing dinoflagellates become particularly abundant. Early interviews with coastal inhabitants revealed that some of the indigenous peoples of the West Coast of North America traditionally posted sentries on cliffs to watch for bioluminescence and suspended shellfish harvesting when it was observed. Even at low concentrations, when waters are not particularly bioluminescent, however, cells can be abundant enough to cause shellfish poisoning. (Photograph courtesy of Botond Szatmáry, http://humpbackbird.com.) ability to provide information in near real time by relaying information about toxic algae to shore using a radio transmitter at the sea surface. MBARI also has tested the protocols and deployed them on ships off California, in the Gulf of Maine and in the Gulf of Mexico, successfully detecting about 10 different species. Scholin s group is working toward the day, not far off, when we can call up the mooring and ask, Are there toxic algae in Monterey Bay, and how high is the toxin level out there? Global Hazard, Global Triumph Focused as we are on harnessing the power of technology to protect ourselves, it s easy to forget that people have always found ways to protect themselves from certain hazards. I was reminded of this fact by a discovery, made during a recent sabbatical, of an approach so obvious that I was later embarrassed not to have recognized it. My sabbatical took me to the Zanzibar Islands, off mainland Tanzania, where I was interested in the likely presence of another genus of toxic algae, Gambierdiscus toxicus. (There exist many more harmful algal species than I can mention in this article.) This dinoflagellate grows on seaweeds eaten by reef-visiting fish; the fish ingest ciguatoxin, the poisonous substance made by the alga. Ciguatera fish poisoning, characterized by a varied combination of gastrointestinal and neurological symptoms, is a public health problem throughout the tropics, but the scientific literature contained no mention of its having been found in Zanzibar, though I discovered it immediately 324 American Scientist, Volume 94

upon my arrival. Why had it not been reported there before? Medical professionals in Tanzania told me they d never heard of ciguatera fish poisoning: It s not around here, they said. But a fisheries biologist visiting the marine station on Unguja suggested I talk with fishermen. I began visiting remote fishing villages with a Swahili translator, a local islander who knew the fish and the local fishing community well. My translator would introduce me to some of the men after they returned in boats from each morning s fishing and sold their catch to fishmongers. After some persuading by my translator, they consented to be interviewed. I asked the fishermen whether they had ever experienced symptoms of illness when they ate certain kinds of fish. Commonly they would say no, not my fish, but they would suggest that there was such illness down the coast. After I compiled a list of what fish were caught in all the villages, I showed individuals pictures of various fish and asked which fish caused problems. Soon a fuller picture emerged. Grouper is a fish commonly associated with ciguatera poisoning. People would say no, there s no problem eating grouper. But I thought to ask whether they had a problem eating the liver of grouper. Liver, a rich source of calories, is highly prized in the Zanzibar islands but when I asked this question, people looked at me as if I were daft. No, they d say, there s no problem with liver. But I continued: Well, did you eat the liver? And they d say no. Why? You don t eat the liver. You get sick vomiting, diarrhea. So there s no problem. And this explained their earlier answer. They avoided the problem by deciding that the liver of grouper was not a food, just as we don t consider the poisonous part of a rhubarb plant to be food. My time in Africa also reminded me that the mouse is not the only organism that has been widely used as a bioassay for shellfish poisoning. In many parts of the world, the bioassay of choice is not a mouse but a cat. It is common in underdeveloped regions to have plenty of stray animals, including hungry stray cats. So you might say that the oldest bioassay is the here, kitty method. A cook calls a stray cat and feeds it a tiny bit of suspect food; if the cat is doing fine in an hour or two, the food is safe to cook. Figure 14. Do some entrenched cultural mores, such as the Torah s prohibition of shellfish consumption as an abomination, reflect an ancient understanding of the hazards of consuming creatures that can be tainted by the waters around them? Evidence is mixed. In the Middle east, for example, some religious groups avoid shellfish; yet during travels in many coastal nations including Turkey, where this Isanbul seafood vendor is selling his product the author found mussels for sale everywhere, despite seeing mussel collectors harvesting in decidedly suspect circumstances. (Photograph by Hakki Sayin, Istanbul, courtesy of the author.) In the industrialized world, we shy from feeding potential poisons to stray cats and have scarce opportunity to check for elderberry ripening or post sentinels to watch our coastal waters for bioluminescence. We must trust science and technology and insist that health and fisheries officials work to keep us safe against a hazard that will probably always be with us. And yet the more we learn about harmful algae, the more we know that coastal people have always lived with them and that a characteristic of each age of human history is the ability somehow to enjoy the rich foods that come from the sea, while managing one way or another to protect ourselves from the poisons in the waters that feed us. Bibliography Bargu, S., and M. W. Silver. 2003. Field evidence of krill grazing on the toxic diatom genus Pseudo-nitzschia in Monterey Bay, California. Bulletin of Marine Science 72:629 638. Erlandson, J. M. 2001. The archaeology of aquatic adaptations: paradigms for a new millennium. Journal of Archaeological Research 9:287 337 Glibert, P. M., D. M. Anderson, P. Gentien, E. Granéli and K. Sellner. 2005. The global, complex phenomena of harmful algal blooms. Oceanography 18(2):132 141. Landsberg, J. H. 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science 10:113 390. Lefebvre, K. A., S. Bargu, T. Kieckhefer and M. W. Silver. 2002. From sanddabs to blue whales: The pervasiveness of domoic acid. Toxicon 40:971 977. Price, D. W., K. W. Kizer and K. H. Hansgen. 1991. California s paralytic shellfish poisoning prevention program, 1927 1989. Journal of Shellfish Research 10:119 145. Scholin, C. A., R. Marin III, P. E. Miller, G. J. Doucette, C. L. Powell, P. Haydock, J. Howard and J. Ray. 1999. DNA probes and a receptor binding assay for detection of Pseudo-nitzschia (Bacillariophyceae) species and domoic acid activity in cultured and natural samples. Journal of Phycology 35:1356 1367. Shumway, S. E. 1995. Phycotoxin-related shellfish poisonings: bivalve mollusks are not the only vectors. Reviews in Fisheries Science 3:1 31. Sommer, H., W. F. Whedon, C. A. Kofoid and R. Stohler. 1937. Relation of paralytic shell-fish poison to certain plankton organisms of the genus Gonyaulax. Archives of Pathology 24:537 559. Wekell, J. C., J. Hurst and K. A. Lefebvre. 2004. The origin of the regulatory limits for PSP and ASP toxins in shellfish. Journal of Shellfish Research 23:927 930. For relevant Web links, consult this issue of American Scientist Online: http://www.americanscientist.org/ IssueTOC/issue/861 www.americanscientist.org 2006 July August 325

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