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How ciguatoxins and other find their way into our chain.

he three voyages that ex- rifying to many. The fact that half plorer, navigator, and car- of the people watching would have tographer Captain James gone blind could only validate any Cook made around the belief in eclipses as portents of evil. world between 1768 and Cook—who ate albatrosses—was 1779 are legendary, not not a superstitious man. There is no T to mention exemplary in indication of foreboding evident in Captain cartographic excellence. Arguably, his journals before the South Pacific his second Pacific voyage was his eclipse of September 6, 1774. least pleasant. Cook eventually met Returning from shore to the ship his demise at the hands of a bunch the following day quite famished, of insulted Hawaiians on his third Cook, along with naturalists Johann voyage. But it was during the sec- Forster and his son Georg, born in ond voyage (1772–75) that he had to 1754, probably relished the thought C ook’s put up with the incessant whining of digging into an unusual-looking of naturalist Johann Forster. And local fish that the crew had ac- it was on this star-crossed second quired from the locals in exchange voyage that he fell ill, twice—once for cloth. The ship’s illustrator was with “bilious colick,” and then with busy drawing the fish, and refused a blocked colon; ran headlong into to allow it to be fired up for din- By Mark Siddall Antarctic ice—twice; and nearly ner. But the fish had been cleaned, died from eating fish—twice! and so the and sacs were After leaving the New Hebri- fair game. After a single bite, the des (today Vanuatu), which Cook trio surely must have thought better claimed for England, the HMS Res- of it. The burning sensation in their olution sailed to the south in order to mouths and throats would have arrive in New Caledonia in time for been immediate. By the wee hours some surreptitious eclipse watching of the morning they were suffering on September 7, 1774. Cook’s care- the full effects of pufferfish poison- ful observations of the Moon’s tran- ing: their skin felt as though it were sit during an annular solar eclipse in a blast furnace while simultane- in 1766 had determined the position ously frosted over with ice, Cook of Newfoundland. Longitude was later wrote. He was oddly incapable terrifically important to navigation. of distinguishing heavy objects from As another eclipse would not be vis- light ones, but that probably con- An oil painting of New Caledonia ible from the British Isles until 1925, cerned Cook less than his constant by William Hodges, first exhibited more such remote eclipse encoun- and involuntary voiding at both in 1778 at the Royal Academy ters were needed. For a variety of ends as progressive set in. of Arts, London. Tasked with recording Captain Cook’s second cultures, a solar eclipse was not to All these terrifying effects resulted voyage, Hodges included Cook’s be taken lightly. Watching the sun from a very slight, mild exposure ship, Resolution, distantly anchored being completely swallowed up by to what is now known as tetrodo- n al Mariti m e Museu Natio and attended by three canoes. the moon seems to have been ter- toxin, a poison that concen-

14 nat u r a l h i s to ry April 2014 April 2014 n at u r a l h i s to ry 15 late Jomon period, in the could get their hands on, it didn’t take long for entrepre- Cook was meticulous with his crew, keeping them first millennium bc, their neurial hibachi-ists to grill whatever scraps they managed on a rigid diet to hold scurvy at bay. One can imagine bones are found scattered to dig out of the trash bins from local restaurants. The a salivating crew dropping anchor in azure blue, cool among those of humans death toll from street-grilled entrails continued to seas resplendent with reef fish. Absent Cook’s stern gaze (though it’s unclear if there mount until General Douglas MacArthur created a strict while he was ashore, the prospect of fresh food roasting was a causal relationship). fugu-licensing program that required safe preparation of on deck would have been a tantalizing and welcome re- Two thousand years later, pufferfish and thorough incineration of their toxic . spite from the daily doses of “antiscorbutic” sauerkraut during the Sengoku, or For some time now, the only deaths from fugu have and spruce “beer” rations. For a crew of 118 they’d Warring Kingdoms, peri- been self-inflicted. The muscle meat of tetraodontid need a lot of fish, though, or at least some big ones. By od (1467–1568), the fish bit fish—named for the two pairs of fused buck teeth form- the time Cook returned to the ship, two huge, reddish- back. Typhoons had twice ing their beaklike jaws, and including more than 120 colored fish had been snagged and hauled on board. spared from Mongol species of pufferfish, globefish, porcupine fish, boxfish, They were promptly cooked and divvied among the invasions in the thirteenth and blowfish—is perfectly safe to eat. Presently, close to crew, with the officers and petty officers getting more century. These “divine ten thousand tons of fugu are eaten in Japan every year, than their fair share, of course. Vegetable side dishes are winds”—the origin of the about half of which is the farm-raised species torafugu, or not noted in Cook’s journal. What is noted is that “in word kamikaze—over- tiger blowfish ( rubripes). Its consumption is more the Evening everyone who had eat of these fish were turned most of the hastily common in the southern regions—there are some 80,000 seiz’d with Violent pains in the head and Limbs, so as built Mongol ships and sent fugu chefs in alone. All fugu chefs are licensed to be unable to stand, together with a kind of Scorch- the surviving crews limp- by a government agency, but only after demonstrating ing heat all over the Skin.” The symptoms of scorch- ing back to their captured mastery of the proper cleaning, preparation, and disposal ing heat foreshadow the same neurotoxic symptoms Korean seaports. The wind of pufferfish. The supposed numbing sensation that is a Cook and the Forsters would experience three months shifted in 1592, however, commonly rumored frisson of fugu is entirely later. According to the account of the ship’s surgeon, when daimyo (warrior-gen- imagined by the patron—perhaps after too much . William Anderson, at least five of the men suffered for eral) Hideyoshi Toyotomi Any actual numbing four days before get- (1537–1598) summoned sensation one experienc- ting back on their feet. the from all over es should be quickly fol- This time, unfortu- Japan to Hizen lowed by hospitalization. nately, the scavenging Castle, on the coast of Ky- What’s more, fugu’s taste animals on board fared ushu island, to rally for a is subtle to the point of worse from eating the full-scale invasion of Ko- being bland. Nonethe- scraps, with the final rea. Having failed, like less, there is apparently death toll amounting Captain Cook, to con- a large culinary niche to one dog, a hog, and sult the locals, a whole that offers $400 plates of a parakeet. regiment of samurai were tasteless fish artfully ar- Ciguatera poisoning felled by their one last big ranged in the shape of a was well known to the Library of Congress Library fish feast the night before chrysanthemum—which Carib people of the A color woodcut titled Pufferfish courtesan and her jellyfish companion, circa 1818–1830, by the Japanese embarkation. The Japanese is, incidentally, a flower Lesser Antilles, who artist Shigenobu Yanagawa. The piece plays upon the allure, and the possible danger, of indulging in fugu. invasions of Korea in 1592 associated with funerals attributed the condi- and 1598 ultimately failed, from Krakow, Poland, to tion to the cigua, a trates in the and reproductive organs of pufferfish. and were disastrous for both countries in terms of casual- Kyushu, Japan. local turban snail (Cit- Although the crew tried, no one could catch the ship’s ties and treasure. But meanwhile, Toyotomi banned the tarium pica) still prized dogs after the poor hounds wolfed down the scraps. consumption of fugu (the Japanese word for pufferfish, everal months today for stews in the Luckily the dogs voided the offending liver on their own meaning “river pig”). Any samurai caught slurping up before the New Virgin Islands. Cigua- A rnis Dez d ins and survived, but a hungry pig that got into the trash the perilous would lose the entirety of his inher- S Caledonian eclipse tera is characterized by Fugu restaurant on touristy Dotonbori Street in Osaka, Japan didn’t make it through the next day. On that following itance. The ban is said to have been overturned 300 years “picnic”—the one that paralysis of the legs, day, local Micronesians, seeing a pufferfish hanging on later, reportedly in 1888, by Japan’s first Prime Minister, nearly extinguished Cook and the two Forsters with uncontrolled salivation, and a burning sensation all deck, frantically pointed and made dramatic gestures to Hirobumi Ito, who apparently took a personal liking to fugu liver—there had been a previous near miss with over. It is interesting to speculate whether the crew of the ship’s crew, which were, no doubt, the Micronesian fugu—and the deaths quickly resumed. a fish, one that remains unidentified, as it was quickly the HMS Resolution experienced ciguatera’s characteris- equivalent of drawing a finger across one’s neck. Post–World War II Japan under American occupa- consumed by a hungry crew. As Resolution reached the tic dyspareunia, a peculiar priapism that is perhaps best tion was not a pleasant place to be. An entire way of tiny and isolated island nation today known as Vanuatu, not fully described in these pages. The poison respon- f Cook had visited Japan during one of his Pacific life was in shambles, the emperor had lost his divinity, which Cook dubbed the “New Hebrides” (he was fond sible for causing such pain, ciguatoxin, would later be voyages, he would have known better than to eat infrastructure and industry were obliterated, and people of antipodean Scottish place names that would annoy the determined to be produced not by the kind of fish that I the livers of these deadly fish. The Japanese have were starving everywhere, especially in the cities. Since French), an “away team” was briefly put ashore to meet Cook’s crew ate, nor by the marine snails that those prized pufferfish for a very long time—as far back as the citizens had no choice but to eat just about anything they the locals. fish might themselves favor, but, instead, by a species of

16 n at u r a l h i s to ry April 2014 April 2014 n at u r a l h i s to ry 17 Coral trout, controllable projectile vomiting, and two were though, instead of their own immune systems dumping Plectropomus maculatus given a good, long bleeding to relieve their throat-choking levels of histamine into their systems, headaches—an approach that could have they had received near-lethal doses of histamine from succeeded insofar as it would have aggra- fish that had been, by all accounts, lying about on board vated their deep shock to the point of pass- for some “number of days”! ing out. The source of this sudden illness was Scombroid poisoning is probably the most common no more a mystery to those present than was illness associated with eating fish. It is also the easiest Cook’s fugu poisoning fifty-four years earlier. to avert. Scombrid fish include various , , All of the afflicted had breakfasted on the same bonito, and wahoo. That scythe of a tail fin attached to a that morning. It is notable that narrow end is characteristic of fish built for speed. These Henderson attributed the sorry state of the fish have evolved a way to deal with lactic acid buildup in fish to having been left overnight “while the muscles that should be the envy of any Olympic sprinter: moon was up,” when in fact the real clue high concentrations of histidine serve as a natural buffer, microscopic lies in his description that for “a number keeping the pH near neutral. At these concentrations, single-celled algae, R . S wainston of days previous . . . everyone had par- though, the histidine is just too tempting for if Gambierdiscus toxicus. several large taken freely of the same fish without suffering the slightest the fish is mishandled or left at room temperature. The Like the algae that are responsible for barques, each of which would be inconvenience.” It is fair to point out here that the mias- histamine by-product is toxic at a measly fifty milligrams toxic red tides, this little critter ebbs and loaded in Leith, Scotland (Old Caledonia, as opposed to matic theory of disease would not give way to the notion per one hundred grams of fish. flows with cyclical oceanic patterns. The prob- New Caledonia), with hardware, merchandise, and muni- of contagion for another half century; it would be another Alas, scombroid poisoning is hardly confined to those lem is bioaccumulation. One little fish eats algae and ab- tions to supply the growing British presence in Australia. twenty-six years before John Snow stole the handle off the species, a fact this author knows from a personal experi- sorbs some ciguatoxin. When a bigger fish eats ten little Each would return home full to the gunwales with sperm Broad Street water pump and stopped an outbreak of chol- ence with a bluefish. Bluefish, Pomatomus saltatrix, is one fish, it retains all of their ciguatoxin. Then huge fish eat oil. One of them, the Triton, was captained by James Crear era cold in its tracks. of my summer time favorites. As an oily fish, it is perfect the big fish that ate the little fish, in turn accumulating in the early 1800s following his exit from the Royal Navy. for grilling; just a little salt and some lemon tame this pre- all of the ciguatoxin all those little fish ate. So it stands to Crear would eventually settle in New Zealand for good, ertain bacteria are able to extract energy from pro- cious piscine pièce de résistance. My first intimation that reason that the biggest and the most predatory fish are go- and at a time when it was an unruly outpost that may well tein instead of sugar by ripping a carbon dioxide off I was in trouble should have been that nagging feeling in ing to have the most ciguatoxin and will be the most dan- have outdone the legendary lawlessness of Deadwood, C of amino acids. In fact, the smell of some cheese the back of my head that I may have somehow way over- gerous to eat, like the big red fish (probably coral trout) South Dakota, some fifty years later. Crear seems and that unmistakable “fishy” smell of, well, spiced the fish, when, in fact, I hadn’t spiced them at all. the crew ate on the Resolution on July 23, 1774—or like to have been a man of considerable charac- My next intimation was total disorientation, wheezing, the barracuda occasionally consumed in the Florida Keys ter, having once saved a fellow captain and considerable homage to a porcelain god. and Saint Thomas that result in the odd death here and who was drowning, and even hav- It is difficult to get a handle on the precise number of there. As for those who don’t die, because they got only a ing taken a principled position cases of scombroid poisoning, and this is a good thing. The minute dose—or because they were put on a respirator in against the “transportation” only poisonings no one tracks are the ones that are rarely time—symptoms of ciguatera can recur for over a decade, (read: “extraordinary ren- fatal, and this is one of them—knock wood, I’m not giving depending on the dose and the individual survivor. dition”) of British prison- Spangled emperor, up bluefish. The connection between histamine poison- Lethrinus nebulosus Ciguatoxin poisoning can happen anywhere. However, ers to the South Pacific ing and improperly handled fish (mea culpa) wasn’t it seems to be concentrated around small, isolated oceanic colonies. With the trade made until the 1940s. Most cases are reported from islands and atolls. The reasons for this remain obscure. routes and shorelines the United Kingdom, the , and Japan. And unlike annual warm-water red tide–related toxins, masterfully mapped out Investigations following a 2008 outbreak of scombroid ciguatera seems to be correlated with the cool phases of by Cook, the Triton could poisoning in Alaska found histamine levels in mahi-mahi El Niño and the Pacific Decadal Oscillation. Too bad for make two return trips a year to that were easily three times the known toxic levels, and in Cook’s crew, then, that Vanuatu is one of the most iso- Tasmania and New Zealand. During a case in the UK, tuna-fish sandwiches that sat on a shelf all lated reef systems on the planet, and suffers even today a one such return trip, on April 17, 1828, some day before they were sold to unwitting victims had more correspondingly enormous problem with ciguatera—es- six hundred miles west of the Azores and more than than fifty times the allowable levels. Still, it is easy enough pecially from eating those very big, reddish reef fish such one thousand miles east of Bermuda, calamity struck. fish is a result of to avoid scombroid poisoning: make your own tuna-fish as coral trout and emperor fish. It is also interesting to note That morning, five members of the Triton’s crew, who this breakdown to amines. sandwich, and, if you didn’t order spicy tuna, ask yourself that it was during one of the strongest Pacific Decadal had until then been feeling just fine, were acutely seized Glutamic acid is broken down why it feels so hot in your mouth.

Oscillations on record that the HMS Resolution plied the with remarkable, if distressing, symptoms, including R . S wainston to glutamine; tryptophan is broken down Pacific. The Hawaiians who killed Cook were “lucky” to violent headaches, capillaries nearly bursting from their to tryptamine; and a few select bacteria, such as the even meet him. bloodshot eyes, and bright red skin. Most alarmingly, their lactobacilli in sauerkraut and yogurt, are able to break Mark E. Siddall is a curator in the Division of In- vertebrate Zoology at the American Museum As a direct result of Captain James Cook’s three voyag- faces and whole bodies were so swollen with edema as down histidine into histamine. Antihistamines had yet of Natural History. His research focuses on the es, each of which included stops in New Zealand, Europe- to render them unrecognizable to their crewmates. The to be invented, so what the five crew members of the biodiversity of leeches and the evolution of their ans were soon frequenting the Tasman Sea and the South- ship’s doctor, Patrick Henderson, sprang to their aid, add- Triton were suffering from was acute anaphylactic shock, hemoxic venoms. This article is adapted from his ern Ocean, hunting whales and establishing a foothold in ing insult to injury. All five received powdered morning- just as severe as if they had all been allergic to peanuts forthcoming book, Poison: Sinister Species with Maori Land. The Australia Company, in particular, had glory root with the immediate, unhelpful effect of un- and had eaten Fluffernutters for breakfast. In this case, Deadly Consequences (Sterling Signature, 2014).

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