Red tide, red terror. Effects of red tide and related ... - ACS Publications

Effects of red tide and related toxins. Dean F. Martin, and Barbara B. Martin ... Publication Date: October 1976. Cite this:J. Chem. Educ. 53, 10, XXX...
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Dean F. Martln and Barbara B. Martin University of South Florida Tampa, 33620

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Red Tide, Red Terror Effects of red tide and related toxins

The term "red tide" is a general one that describes the sudden proliferation of microorganisms, typically in the marine environment, that give rise to discolored water and other phenomena (including mass mortalities of marine animals, paralytic shellfish poisoning, severe economic losses, and respiratory and contact irritation). In addition, there have been 1600 known cases of human intoxications associated with the red tide, with about 300 fatalities. By comparison, more than 300 persons in the United States alone were stung to death by bees and wasps in a recent year (I).In the US., no more than 12 deaths have been caused by snake venoms, during the past five years, despite 45,000 snakebites occurring annually (2). Many believe that red tides are a phenomenon that has been with us through much of recorded history and tradition. Rachel Carson noted (3),for example, that west coast Indians would recognize the dangers of red tide blooms, particularly in mussel poisoning for generations before white men appeared, and when the red streaks would appear on the sea, guards were stationed on the shore to prevent the taking of the mussels until the warning signals had ceased. Inlanders were thus warned who might be unable "to read the language of the sea." Some have suggested that the phenomenon may have been described in the Bible (3) and all the waters that were in the river were turned to blood. And the fish that was in the river died; and the river stank, and the Egyptians could not drink of the water of the river and there was blood throughout all the land of Egypt. Admittedly, sudden proliferation of single-celled plants or algal blooms represent a biological phenomenon. But, the organisms live in a chemical environment that is on the average a 3.5 weight percent solution of dissolved salts (85% NaC1) with chemical nutrients, and the materials that are responsible for massive marine intoxications and paralytic poisoning are chemical substances that attract, if not command, the interest of chemists.

Summaw of Some Toxigenic Organisms Organism

Gonyoulox cotonello Gonyoulax,tamarensis (G. excauoto) Gonyoulox ocarenella Gonyaulax monilota Gymnodinium breve Gyrnnodinium veneficum Prymnesium pnrvum

Location

T y p e of Organism armorea dinoflagellate dinoflagellate dinoflagellate dinoflagellate unarmored dinoflagellate dinoflagellate crysomonad

PaCifiC Coasts. U.S., and Canada Bay o f F u n d y , south t o N e w England Bay o f F u n d y G u l f o f Mexico Gulf o f Mexico English Channel Mediterranean Sea. Europe, and M i d ~ a s fresh t water

with red tides in the United States are probably more severe than any other nation in terms of the public health problem and the-economic impact. What Does a Red Tide Do? These organisms have four different toxic effects. Mass Mortalities Due to Oxygen Deprivation

As any red tide organism dies, biochemical decomposition occurs, and oxygen levels can become rapidly depleted. For example, approximately 100 species of marine animals are known to have been killed by the Florida red tide organism, Gymnodinium breue ( 4 ) , and a considerable fraction has been due to the oxygen-depletion effect (separateexperiments have shown that the death of barnacles and other creatures was due to oxveen ." deorivation. not toxin (5)).Those killed include fish (trash, commercial, sport), shellfish (shrimp, oysters, crabs), some birds, porpoises, turtles, barnacles, and even invertebrates (sponges).Entire bottom communities were completely devastated in Tampa Bay during a spread of red tide in Tampa Bay in July 1971 (6). In contrast the "mahogany tides" that are responsible for fish kills in Chesapeake Bay, are associated with non-toxic dinoflagellates; the possibility that bacteria in the dinoflagellate patches initiate the fish kills has been considered (7,8).

Occurrence of Red Tide One type or another organism is responsible for red tide throughout the world from Antartic waters to the Norwegian fjords. The persistence of the phenomenon is evident from the geographical names that arise from it. The Red Sea gets its name from one common, persistent bloom or red tide organism (Oscillntoria erythraea), the Gulf of California was once known as the Vermillion Sea because of the persistence of another organism. In the United States, all coastal waters have one type of red tide organism or another; some are a greater problem than others; the toxigenic organisms contain within them a poison or toxin of varying potency and characteristics. These are summarized in the table. The problems associated

In Florida mass mortalities of fish and marine animals occur because of a toxin that is associated with the red tide organism, G. breue. In Massachusetts, the onset of the 1972 red tide was indicated by the death of some 95 sea birds (the deaths were due to paralytic shellfish poisoning). The massive nature of fish mortalities in Florida is difficult to describe, but data for the city of St. Petershurg alone may help: during February ItLMarch 18,1974 as many as 150 men worked in 8-hour shifts to clear the beaches of dead fish (costs were estimated to exceed $160,000).This was for a comparatively minor outbreak

1 The choice of title might seem overly dramatic, but for the fact that a distinguished chemist at Iowa State once mistakenly asked about our progress in research on "the red Terror," and after thinking about the implications of red tide outbreaks, his slip of the tongue seemed an apt one. Research on toxins from G,tamarensis has heensummarized by Prakash (26),Sehantz and coworkers (19), and Shimizu and eoworkers (27). Research on toxins from G. breve also have been summarized (28-30). The toxin from G. brew appears to be unique hecause of the hemolytie activity which may be responsible for acute mortalities of fish (311.

Shellfish (oysters, clams, mussels) may ingest a toxin-containing red tide organism and mechanically entrap the persons who coniume the contaminated shellfish become afflicted with paralytic shellfish poisoning and death may result, depending upon the number of shellfish, the degree of contamination, the species of the red tide, the recency and intensity of red tide. The dangers posed by paralytic shellfish poisoning (PSP)

614 / Journal of Chemical Education

Mass Mortalities Due to Organism-Associated Toxins

Shellfish

are very great, as indicated by the description of symptoms noted for infestations by Gonyaulax tamaremis (10) [The] poison is. . .50 times as potent as the paralytic poison curare. About 30 minutes after eating contaminated shellfish, PSP victims experience gastrointestinal distress, burning sensations, and in severe eases ataxia, respiratory paralysis, and cardiovascular eollapse. Death can come within 12-24 hours. No antidote to the tmin is known; treatment is largely symptomatic. Cooking of shellfish meat only partially reduces its toxicity. A lethal dose of poison can be contained in as few as three fried clams. The world wide incidence of known PSP to humans bas been estimated to he about 1600 cases, including 300 fatalities. Additionallv. a number of cases of mortalitv of domestic animals, fish, birds, and other marine animals'have been linked directly with PSP. (The economic effect of PSP is considered separately in the next section.) The severity of PSP depends considerably upon the organism. No fatalities have been recorded for the Florida red tide organism, though about 150 fatalities associated with PSP have &en estimated for Pacific coast organism, Gonyaulax catenella, in California and Alaska. Considerably fewer fatalities associated with P S P have been observed for northeastern United States and Canada. In part the reduced fatalities have been due to education of the public andlor enhancement of shellfish poisoning management. The predictive characteristics are still limited, with some interesting exceptions. I t is a tribute to management by state officials that the anticipated 20% fatalities (10) have not in fact been observed in the New England area. Discomfort Due to Air-Born Aerosols In Florida coastal waters, Gymnodinium breue, an unarmored dinoflagellate, is destroyed in the surf, and it appears that the resulting aerosols contain irritating substances that cause respiratory problems for persons up to 3 M 0 miles from the red tide bloom. Literally thousands of persons are affected. The irritant is virtually odorless, and the attack is characterized by an initial paroxysmal coughing with tearing and rhinorrhea from irritated eyes and nasal passages (11). The problem is alleviated almost immediately upon leaving the beach area, hut it is also ohvious that a considerable number of persons come to Florida specifically to spend time on the beaches, not away from them. What is the Economic Impact of a Red Tide Bloom?

Data concerning the economic impacts are hard to acquire hut the following information should indicate the scope and magnitude of the problem ( 8 ) New England The first red tide in recorded Massachusetts history occurred in 1972, and the establishment of "seed beds" of the organism would indicate the possibility of future outbreaks, and, in fact, outbreaks also occurred in 1973 and 1974. The final human toll was 26 illnesses, two classified as severe, no deaths. The economic impact in 1972 arose from the fact that 2.800 acres of Massachuietts shellfish harvesting ihoreline were contaminated, and state officials instituted a courageous. aggressive program to prevent exportation of contamhated shellfish. The digging ban lasted a month in Massachusetts (and a week in Maine). Loss was estimated to be 1 million dollars by the National Marine Fisheries Services because of adverse nublicitv that denressed the market. Clam dizeers -received'unempioyment compensation of $47/wk, though a good digger could earn $27-36lda in season (12).

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New York A bloom did not occur in New York waters, but the state was economically afflicted by the "halo effect" from New England adverse publicity in 1972 (12). The halo effect is the damage

Figure 1. Areas of Florida most con.monly affected by blooms of Gymnodinium breve.

to those portions of the fishing industry not directly involved in the PSP outhreak. In New York, the wholesale price of clams from Long Island and other a f f x t e d areas fell by 25% during the PSP outhreak in New England. The item is significant because about 50% of the hard clams produced in the United States are harvested in New York marine waters, and the value in New York City frequently governs the value elsewhere. Alaska An entire shellfish industry in Alaska has been affected by PSP problems. In the 1945-46 season, for example, a peak of 260,000 pounds of canned and frozen butter clams were produced by Alaska (13). These were adulterated by poison from red tide organisms; the seizure of the lots of clams devastated the industry, and after five years, it became ohvious that the costs of quality control and area management were simply prohibitive. Alaska, then and now, simply does not have any butter clams that are certified for interstate shipment. Florida Since 1971, Florida has experienced two red tides, and neither has caused serious PSP conditions because of good management and because the responsible organism, G. breue, is ordinarily separated from shellfish by an ecological barrier of different salinity regimes. In Florida the economic impact of both red tides has been significant along the west coast where the organism typically blooms (curiously, no significant outbreak bas ever been ohserved along the east coast). The range of affected areas is indicated in Figure 1. The outhreak in 1971 lasted three summer months and affected seven counties from zone 1-6, the figure. It was of moderate severity, short duration, and widely publicized. The total loss to the tourist industrv was t found he $18,000,000 according to Habas and ~ i l h e r (9 a,b), and total clean-up costs brought the total to $20 million. The red tide of 1973-74 was sporadic, occurred during peak tourist season, was widespread, hut fortunately national publicity was minimal. The economic damage was due to the prolonged severity. Hbas and Gilbert (1975) estimated that the damage to the tourist industry alone was $15 million, and data are being collected on damage to the real estate industry. Volume 53. Number 10, October 1976 / 615

What is the Economic Impact of Red Tide on a Non-Red Tide Area?

No satisfactory answer is available for this question. The halo effect was described for New York, and it exists elsewhere. For example, the sale of fish in Florida seems to decrease during a red tide outbreak, even though the fish are imported from elsewhere in the United States or even abroad. In 1972, clams from New England were recalled from the shelves of supermarkets in Florida and throughout the country. I t would appear then, that red tide outbreaks in New England, California, along the Gulf coast, and even on the Atlantic coast do have a highly local impact, but the effects can be felt inland to some unknown extent. How Do Toxic Red Tides Affeci Man and Marine Animals?

There are several answers to this question, and some have already been provided. Red tides affect man economically, socially, esthetically, as noted earlier as well as physiologically. There appear to be three significant toxigenic algae that are particularly troublesome in U.S. coastal waters. The toxins from these algae have been characterized to differing degrees, both chemically and physiologically.2Some species of Gonyaulax, notably G. catenella and G. tamarensis (properly G. excauata, according to Loeblich and Loeblich (14) produce paralytic poisons, and saxotoxin from G. catenella is probably characterized. Saxotoxin has been isolated from Alaskan butter clams (Saxidomas giganteus), California mussels (Mytilus californianus), and from axenic cultures of G. catenella (15). Purification was effected by ion exchange chromatography using carboxylic acid resins, followed by chromatography usingacid-washed alumina (16). The products obtained from three different sources have remarkably consistent properties. For example, the potency is measured in terms of mouse unitslmg of poison, and the values obtained were 5,200 (clam poison), 5,300 (mussel poison), and 5,100 MUImg (G. catenella poison) (15); all were within the experimental error value of 5,500 f 500. The infrared spectra, nitrogen content, specific optical rotation, and pK, values were identical (within experimental error) for saxotoxin from all sources (c.f. 17). In addition, saxotoxin was isolated from a fresh-water blue-green alga, Aphanizonomenon flos aquae (18). Finally, Schantz and co-workers (19) noted speculation that a poison produced by G. tamarensis may convert to saxotoxin upon aging in acid solution. Thus, the distribution of saxotoxin is widespread in the environment, and it may well be that this compound is the result of a degradation of ametabolic product. Purified saxotoxin is isolated as a white hydroscopic ma= 8.2 and pK,n terial that is a water-soluble dibasic salt = 11.5). It has been isolated as the hydrochloride and the elemental composition was CloH170N704.2HC1 (15). No ultraviolet absorption was observed. Positive Benedict-Behre and Jaffe tests were reported, and the compound was completely detoxified by mild catalytic reduction (uptake of 1 mole of hydrogenlmole of compound at atmospheric pressure). A crystalline derivative with p-bromohenzenesulfonic aeid was obtained and crystallographic analysis established the structure of saxotoxin (Fig. 2) that appears to he compatible with all known characteristics of the molecule (19). Descriptions of saxotoxin toxicity in humans vary (20). The most characteristic effects, paresthesias and paralysis, appear shortly after ingestion of contaminated shellfish. Oral mucous membranes are affected first, then the extremities, and ataxis and vertigo follow. Various central symptoms have been renorted. including grippinp . . . sensation of the throat, stiffness k d in thr nuchal region, and drynt:~; oi the pharynx, sneech im~whcrence,and complete aphasia. Hypoteniion is observed only with greater dosages. Survival beyond two hours is considered a favorable prognostic sign. No antidote has been discovered up to 1975. 616 / Journal of Chemical Edocafion

Figure 2. Structure of saxotoxin (19)

Probably the guanidinium moiety present in the saxotoxin molecule is a key to understanding the mechanism of some of the significant dhysiologicalchara&ristica (21). Guanidinium ion (H2N)&=NH2+ in isotonic concentration can restore the ability of sodium deficient cells to conduct impulses, and because of its size, guanidinium ion can mimic sodium ion, and guanidines may produce rhree act as 3 carriw. %-subs~ituted different modificatiuns: (1, reduced ability 11, restore excnahilit\.. 121inhibitimuf theal)ilitvofsodium ionur cuanidin. ium ion to restore excitability, and (3) development of antagonistic effects without depolarization. I t appears that saxotoxin interferes with the movement of the sodium ion much as substituted guanidinium ions can: reducing numbers of membrane channels through which sodiummoves (22). Saxotoxin is qualitatively similar inaction to local onestheric agents cuch a i cocaine and prwainc though a l ~ o ulGO.000 ~ times more potent. I h t cocaine and procaine interfere &th movements df potassium ion. The interferences of saxotoxin with Na+ channels seem to be stoichiometricone toxin with one channel (23). Thus though the substituted guanidinium picture suffers from the danger of simplicity, it also has the advantage of clarity. Saxotoxin has had a curious history. Obviously, it has caused much misery. Hearings before the U.S. Senate committee brought out its potential use in biological warfare. But its use as a model compound in physiological studies is perhaps best kept in mind. For example, based upon the stoichiometric relationship mentioned earlier, it has been possible to estimate the numbers of channels in excitable membranes as 13/pm2 of membrane surface in the walking leg of the lobster, and 75/pm2 (24) in the cervical vagus nerve of rabbit (25). Saxotoxin is, indeed, a most promising potential as an experimental tool.

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Acknowledgment

Our research on the red tide problem was greatly assisted by a P H s Career Development Award (to D.F.M.) from the National Institute of General Medical Sciences. Initial research support was provided by the National Marine Fisheries Service (NOAA). Literature Cited (1) Gi1bert.P. W., cited by Fanning. P . i n Notional Obremei 8 I28 June 19751.

(2) Russell, F.E.,Carlron.R. W.. Wainschel.J..andOsbi~me.A.H., J. Amrr Mrd Ass., 233,341 119751. (3) Carson, R.. 'Thesea Amund UCSignet. New York. 1 9 6 1 , ~ 45. . I41 Sfoidinger. K, A,. Burkey. M. A , and Inglc, R. M . i n "Marine Pharmacwnoay." (Editors: Martin,D. F..andPadilla.G.M.l,AcadcrnicPrers. Inc..New York. 1973.Chap. ".I

..

I51 Sievors, A,, J. Proto2ool.. 16,401 119691. 161 Simon. J.L..andDauor,D. M.. Enilirnn. Lett., 3.229 119721. (7) Se1iger.H. H.. Lofws,M. E., and Subba Rso,D. V.,Proc. 1st. Ire( (81, pp. 181-2051. R, i~dim). PIOC ist ~ ~ t ~ . ~ ~ ~ r . ~ ~ ~ i ~ ~ i ~ ~ f l ~ ~ ~ ~ ~ a t e ~ (81 Techno1 Found.. Wakelurd, 1975. I91 Hahsr, E.J.. and Gilherf.C., ref IR1.p. 99:ci..Enuirnn. Lett., 6.139 119741. (lo) Piakash,A..Medcd,.l.C..and Tannant.A. D.."ParaiytieShell(irh Poisoning in Eastern Canada." Fisheries Remarch Board of Canada. Ottawa. 1971. 1111 Hernrnerf. W. H.. rei. lRl.p.489. 112) Jonsen, A. C., ref. (81,p. 507. 1131 Clem. J. D., ref 181, p.469. 1141 Loeb1ieh.L. A,. andLoehlich, 1ll.A. R.,reiIRl,p. 207. 1151 Sehanfz.E.J..l.vnch.J. M..Vawsda,G..MsUumofo.K..andRapopurt.H..Aio~h~m.. 5,11911196fii (16) Schantz. E. J., Mold. J. D., Stanger. D. W. Shauel, J.. R i d F.J. B0vden.d. P.. Lynch. J. M., Wyler, R. S.. Riegel, R., and Snmrner, H., J. Amri. ('hem. Sac., 79, 5250 1,9571.

(17) Noguehi. T.. Konnu, S.. and Hashimato, Y.. Toricon. 7.325 (19691. (181 Jackim. E., and Gentile, J., Science. 162,915 119681. (191 Sehantz, E. J., Ghazarassian, V. E.. Schnrrs. H. K.. Strong, F. M., Springer, J. P., and Clardy, J., r o t 181, P. 267, c/. J. Amsr Chem. Soc.. 97, 1238 Peuanite, J. 0.. (19751. (20) Bull, R. J., and Pringle, B. J.. in"Drugs from the Sea." (Editoc Freudenthal, H.D.1, Marine Tech. Soc.. Washington, 1968, pp. 7e-80. (211 c/. DDg, M. T.. 111. Martin, D. F.,snd Padilis. G. M.. in "Marine Pharmacognny," (Edilor8:Martin.D. F.,and Padil1a.G. M.IAesdamiePresr,Now York, 1974,Chap.

I. (22) Kso, C. Y.,in "RioactiueCompaundafrom t h e s s ? (Editors: Humm. H. J..snd Lane,

C. E.1,Dekker. NewYork. 1971.Chap. 5. (23) c/. Cueruo,L. A.,and Adolman, W. J., J. Cen. Phwiol.. 55,309 (1970). Ilnndoni, 188,99(19671. (241 M0ore.J. W.,Nsreha~hi,T..andShaw.T.I.,J.Physiol, (251 Keynes, R. 0.. Ritehie. J. M..and Rujar, E.. J. Phyxioi.. 2L3,235 (19711. I261 Prakash. A,. J. Fish. Res. Ed. Con.. 24, 1599 119671. I271 Shimizu, Y., Alam. M.. and Fallon, W. E., ref. 181, p. 275. (281 Martin,D. L a n d Martin. H.H., r e t ( B ) , p267. I291 Padil1a.G. M., Kim, Y. S.,and Martin, D. F.,ref, (81, p. 199. (30) T r i ~ f fN. , M..Ramanujam. V. M.S.,Alam,M.. Rsy.S. M..andHudson,J. E.ie1. I81 p. 309. (311 Kim, Y. S.,Linton,J. %andMartin, D. F.. Toricon. 12,439,1974.

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