• TABLE OF CONTENTS
HIDE
 Title Page
 Table of Contents
 Introduction
 Types of fish poisoning
 Symptomology and public health...
 Geographic distribution
 Species reported as ciguatoxic
 Chemistry and pharmacology
 Biogenesis and transmission of...
 Effects of ciguatera poisoning...
 Summary and conclusions
 Acknowledgements
 Bibliography
 Appendix






Title: Fish poisoning in the eastern Caribbean
CITATION PDF VIEWER THUMBNAILS PAGE IMAGE ZOOMABLE
Full Citation
STANDARD VIEW MARC VIEW
Permanent Link: http://ufdc.ufl.edu/UF00096172/00001
 Material Information
Title: Fish poisoning in the eastern Caribbean ciguatera study
Physical Description: 39 p. : maps ; 28 cm.
Language: English
Creator: Brody, Robert W
Caribbean Research Institute
Publisher: Caribbean Research Institute, College of the Virgin Islands
Place of Publication: St. Thomas, U.S. Virgin Islands
Publication Date: 1971
Copyright Date: 1971
 Subjects
Subject: Poisonous fishes -- Caribbean Area   ( lcsh )
Fishes -- Caribbean Area   ( lcsh )
Genre: bibliography   ( marcgt )
non-fiction   ( marcgt )
Spatial Coverage: United States Virgin Islands
 Notes
Bibliography: Includes bibliographical references (p. 39).
General Note: Cover title.
General Note: "For presentation: 24th annual session, Gulf and Caribbean Fisheries Institute, Miami, Florida, 15-18 November, 1971."
Statement of Responsibility: Robert W. Brody.
 Record Information
Bibliographic ID: UF00096172
Volume ID: VID00001
Source Institution: University of the Virgin Islands
Holding Location: University of the Virgin Islands
Rights Management: All rights reserved by the source institution and holding location.
Resource Identifier: oclc - 04391928

Downloads

This item has the following downloads:

PDF ( 8 MBs ) ( PDF )


Table of Contents
    Title Page
        Title Page
    Table of Contents
        Table of Contents
    Introduction
        Page 1
        Page 2
    Types of fish poisoning
        Page 3
        Page 4
        Page 5
        Page 6
        Page 7
        Page 8
        Page 9
    Symptomology and public health aspects
        Page 10
        Page 11
        Page 12
        Page 13
        Page 14
        Page 15
    Geographic distribution
        Page 16
        Page 17
        Page 18
        Page 19
        Page 20
    Species reported as ciguatoxic
        Page 21
        Page 22
    Chemistry and pharmacology
        Page 23
        Page 24
        Page 25
    Biogenesis and transmission of ciguatoxin
        Page 26
        Page 27
        Page 28
        Page 29
        Page 30
    Effects of ciguatera poisoning on the development of fisheries
        Page 31
        Page 32
        Page 33
        Page 34
        Page 35
    Summary and conclusions
        Page 36
        Page 37
    Acknowledgements
        Page 38
    Bibliography
        Page 39
    Appendix
        Page 40
        Page 41
        Page 42
        Page 43
Full Text






CARIBBEAN RESEARCH INSTITUTE


FISH POISNNG IN THE ES ARIEAN


Robert W. Brody

Ciguatera Study
Caribbean Research Institute
College of the Virgin Islands
St. hxamas, U. S. Virgin Islands 00801








Pe Presentation

24th Annual Sessin
Gulf and Carilxian Fisheries Institute
Miami, Florida


15-18 Novenber, 1971










CONTENTS


Page

I. INTRODUCTION 1


II. TYPES OF FISH POISONING 3


III. SYMPTOMOLOGY AND PUBLIC HEALTH
ASPECTS 10


IV. GEOGRAPHIC DISTRIBUTION 16


V. SPECIES REPORTED AS CIGUATOXIC 21


VI. CHEMISTRY AND PHARMACOLOGY 23


VII. BIOGENESIS AND TRANSMISSION OF
CIGUATOXIN 26


VIII. EFFECTS OF CIGUATERA POISONING ON
THE DEVELOPMENT OF FISHERIES 31


IX. SUMMARY AND CONCLUSIONS 36


X. ACKNOWLEDGEMENTS 38


XI. LITERATURE CITED 39









INTRODUCTION




"When I first got here I thought that I would be able

to practically exist on fish....."; "I was poisoned fifteen

times before I left my father's house. He always liked to buy

big fish because there was more meat..... "; "I can't get a

contract for grouper or snapper with any of the hotels. They

buy the same fish from Santo Domingo for ten cents a pound

more..... "; "Where are all the seafood restaurants ? I thought

this was an island !"


These comment s and others like them represent a

biotoxicological problem which has always plagued the eastern

Caribbean. Ciguatera fish poisoning, scombroid poisoning,

and to a lesser extent "clupeoid", tetraodontoid and elasmo-

branch poisoning have been reported since pre-Columbian time

and the problem shows no sign of lessening.


This paper will present the basic facts of fish poisoning

in the eastern Caribbean area as we presently know them. It

will not attempt to review the voluminous literature from the

Pacific; the reader is referred to excellent s u m mi a r i e s of


-1-









Halstead (1967) and Banner (1971). At the present time we have

very little "hard data" on the chemistry, biogenesis and biology

and pharmacology of the fish poisoning problem in the area.

We have yet to confirm that the most important type of poi-

soning, ciguatera, is in fact identical to the toxin from the

Pacific. The sections on ciguatera are therefore based on our

local observations and inferences from studies in the Pacific

are noted.


-2-









II. TYPES OF FISH POISONING


Fish poisoning in the eastern Caribbean can be broken

down into three major groupings. The endotoxins from the puff-

er-like fishes with the additional rarely reported cases of

clupeoid, elasmobranch and hallucinogenic fish poisoning form

the first group. These incidents represent a very small per-

centage of the total number of cases reported; several years

of casual data-gathering and six months of active research have

only produced two accounts in the last four years, both of

clupeiotoxism.


The biology, chemistry, and pharmacology of puffer

fish poisoning have been accurately summarized else whe re

(Bagnis, 1970). Although the world-wide fatality rate is high

(61%), very few cases oftetraodon poisoning are reported in the

Caribbean, probably because the puffers are not highly esteemed

as a food fish. This may also be the reason for the low in-

cidence of reports of elasmobranch poisoning in the area.

Shark has been harvested recently in an effort to produce a

packaged seafood product ("Sea Flake") with generally good

customer acceptance; there have been no instances of elasmo-

branch poisoning brought to our attention as a result. Hallu-









cinatory fish poisoning (icthyoallyeinotoxism) is also an ap-

parently rare event in the eastern Caribbean; it has been

described to us by an herbalist on St. Thomas but an actual

case history has not been received.


Cleupeoid poisoning is a form of icthyosarcotoxism

caused by ingestion of the flesh of fishes of the order Clu-

peiformes. The symptoms are frequently violent with an ex-

tremely high case fatality rate. The onset of symptoms is

noted with a sharp, metallic taste in the mouth followed rapidly

by severe gastrointestinal upset with distinct indications of

vascular collapse (drop in blood pressure, cyanosis). This

may be accompanied or rapidly followed by neurological dis-

turbances nervousness, dilated pupils, violent headache,

tingling, and in severe cases respiratory distress, convulsions,

coma, and death. The toxin is apparently particularly virulent:

death may occur within fifteen minutes. The literature reports

that persons have died while in the act of eating the fish "part

of the fish was still in the victim's mouth at the time of death"

(Halstead, 1967).


Fish in the families Clupeidae (herrings), Engraulidae

(anchovies), Alb ul idae (bonefishes), and Elopidae tarponss)








have been reported as toxic in the Caribbean; our experience

has been limited to two cases involving the clupeoid fishes

Herengula humeralis (ye llo w b ill e d sprat) and Opisthonema

oglinum (thread herring). One case is reported from a fisher-

man on Tortola, B. V. I. who (with his family of five) ate "yellow

bill sprat" (probably Opisthonema oglinum from his descrip-

tion of a "spine on the back fin") caught in Great Harbor, Peter

Island, B. V. I. He reported "bad fish poisoning" symptoms

generally similar to ciguatera poisoning; the rapid onset re-

ported above was present. He forced all of the members of his

familyto vomit and alltook a "heavy dose of sulphur" (a patent

medicine). He did not contact public health authorities. The

family recovered from acute symptoms within 36 hours. (This

incident took place in late 1967 and was reported in April 1971;

the interview was thus clouded by time and at least two subse-

quent incidents of ciguatera poisoning. ) The second case is

reported byHalstead (1970) from Antigua, W.I. from 1968 (?)

when "some small surface-feeding 'herring-like' fish were

eaten". Two people died in this outbreak. Halstead suggests

that local terminology of "yellow-billed sprat" is applicable to

llerengula humeralis. The violence of the episode suggests

that this case was an example of classic clupeiotoxism while

the Tortola case is not definitely separable from ciguatoxism .










The chemical nature and biogenesis of clupeiotoxism

is not presently known. Numerous authors have suggested that

fish caught during the summer months are more likely to be

toxic. All reported incidents are from fish caught close to

tropical islands. There are several references in the literature

to planktonic blooms as the causative organism, specifically a

monadd" (dinoflagellate ?) (Halstead, 1967), Skujaella,

(Trichodesmium) (Randall, 1958) or to "swarming of palolo

worms" (Halstead, 1967). It is probable that the toxin is pro-

duced by some planktonic form as the clupeoid fishes are for

the most part plankton feeders, this may add strength to the

position that clupeiotoxism is a separate entity from ciguatera

poisoning. Clupeiotoxin is not thought to be degraded by normal

cooking and the degree of freshness does not seem to have effect

on the toxicity.


Clupeiotoxism may pose a wider threat to public health

than the occasional locally consumed fish. If the toxin is in-

deed caused by "blooming" plankton organism the likelihood of

a large school of toxic fish cannot be overlooked. The sardine

and anchovy groups are frequently thought of as ideal fish for

Fish Protein Concentrate production; we have no data on the

ability of current FPC technology to eliminate the toxin from


-6-










the raw fish.


The second major group of poisonings experienced in

the eastern Caribbean is the result of bacterial decomposition

of fresh fish. In the Virgin Islands and throughout the northern

Leeward Islands fish are typically sold "fresh" from the boat.

Very few fishermen use ice or gut the fish before sale, in fact

there is a strong feeling among older citizens that such pre-

servation is usedto camouflage the true "freshness". Eastern

Caribbean fishermen do not use live-wells and fish frequently

spend a good part of the day in the sun. These conditions ob-

viously tend to promote bacterial decomposition of the fish and

the consequent toxicity problem; it is interesting that the younger

people in St. Thomas, U. S. V. I. who tend to buy fish in the

supermarket report a significantly lower incidence of fish poi-

soning attributable to scombroids.


We presume that an undetermined proportion of the

poisonings reported are the result of some sort of bacterial de-

composition. In many "mild" cases the only complaint is of

gastrointestinal distress; the neurological symptoms specific

to ciguatera and ciguatera-like toxins are not noted. Many of

these cases may be attributable to scombroid poisoning but the

symptoms may not be sufficiently pronounced for a proper









diagnosis to be made.


The distinct histamine-like toxicity caused by bacterial

degradation of the flesh of fish of the family Scombridae is a

relatively common type of fish poisoning throughout the Carib-

bean. The symptomology includes a distinct "sharp" or

"peppery" taste upon eating the fish followed by intense head-

ache, dizziness, a variety of circulatory disfunctions, gastro-

intestinal distress, dryness of the mouth, and inability to

swallow. These symptoms are followed by generalized

erythema, the face becomes swollen and flushed, eyes are

sunken, and an urticarial eruption may develop covering the

entire body. In severe cases there may be additional compli-

cations of shock and respiratory distress. Death has been re-

ported in a few cases but acute symptoms generally dissipate

in eight to twelve hours. This toxic reaction is brought about

by the bacterial degradation of histidine in scombroid muscle

tissue which produces a substance designated as scombrotoxin.

Scombrotox in probably has a combination of chemical con-

stituents including saurine, histidine, and possibly other toxic

compounds. The disease responds well to treatment with anti-

histaminic drugs; this specific treatment has mitigated the

severity of scombroid poisoning as a public health problem in

recent years.







In the eastern Caribbean scombroid poisoning has been

reported from Acanthocybium solandri (wahoo) Scomberomorus

cavalla (kingfish or king mackerel). Scomberomorus regalis

(spanish mackerel), and S. maculatus (cero). We are not aware

of cases reported recently from the eastern Caribbean in the

tunas (Auxis, Euthynnus, Sarda, Scomber, Thunnus) but these

genera may also be incriminated. There probably is no true

seasonality to scombroid poisoning although the incidence in any

one area can be correlated with local "runs" of the particular

species involved. Thus there seem to be more poisonings

during the tourist season when sport fishing pressure is high.


The third general type of fish poisoning is described

as ciguatera fish poisoning. Evidence from the Pacific suggests

that there are at least three (probably more) distinct toxins

capable of producing the ciguatera syndrome. Many authors

(and many physicians in the eastern Caribbean area) have not

separated the diagnosis or treatment of ciguatera from that of

scombroid poisoning and some confusion has resulted. Both

ciguatera and scombroid poisoning have been occasionally re-

ported from the same fish in the Pacific (Halstead, 1967); we

have no such report from the Caribbean in recent years.


-9-








III. SYMPTOMOLOGY AND PUBLIC HEALTH
ASPECTS OF CIGUATERA



In the absence of precise chemical and biogenic data

we have defined ciguatera in terms of its symptomology. The

following symptoms are extracted from Halstead (1967), Bag-

nis (1970), and Banner (1971) and are quoted as they appear in

Teytaud and Brody (1971):


"Ciguatera fish poisoning in its simplest un-
complicated form develops within 3 to 5 hours after
the fish is eaten. There is a sudden onset of abdominal
pain followed by nausea, vomiting, and a watery diar-
rhea. The gastrointestinal symptoms will occur in
about 40 to 75 percent of the cases. The victim feels
weak, generally ill, and may experience muscle aches
throughout the back and thighs in about 10 percent or
more of the cases. Soon after, the victim complains
of numbness and tingling in and about the mouth which
then extends to the extremities (present in about 50
percent or more of the cases). Fever, headache, and
rash are generally absent, and the patient has no de-
sire for food. The acute symptoms usually subside in
about 8 to 10 hours, and within 24 hours after onset
most of the patient's symptoms will have completely
subsided except for a feeling of weakness. However,
the numbness andtingling may continue to lesser ex-
tent for a period of 4 to 7 days. The foregoing re-
sume is typical of the majority of uncomplicated
ciguatoxications that are generally encountered by the
practicing physician in an endemic ciguatoxic locality.

Ciguatera, like many other d i s e a s e s, may
vary greatly in its clinical manifestations depending
upon the toxicity of the fish that is eaten, the individ-
ual's sensitivity to the poison, amount of fish ingested,
and other factors. In a broader sense ciguatera fish
poisoning may be characterized as follows: the onset


-10-







of symptoms may vary from almost immediately to
within a period of 30 hours after ingestion of the fish,
but is usually within a period of 6 hours. The initial
symptoms in some cases are gastrointestinal in nature,
consisting of nausea, vomiting, watery diarrhea a,
metallic taste, abdominal cramps, and tenesmus,
whereas in other patients the initial symptoms consist
of tingling and numbness about the lips, tongue, and
throat. This may be accompanied by a sensation of
dryness of the mouth. The muscles of the mouth,
cheeks, and jaws may become drawn and spastic with
an accompanying sensation of numbness throughout.
Generalized symptoms of headache, anxiety, malaise,
prostration, dizziness, pallor, cyanosis, insomnia,
chilly sensations, fever, proiuse sweating, rapid
weak pulse, weight loss, myaigia, and back and joint
aches may be present in varying degrees, or one or
more of the symptoms may be entirely absent. The
victims usually complain of a feeling of profound ex-
haustion and weakness. The feeling of weakness may
become progressively worse until the patient is unable
to walk. Muscle pain are generally described as a
dull, heavy ache, or cramping sensation, but on
occasion may be sharp, shooting, and affect particu-
larly the arms and legs. Victims complain of their
teeth feeling loose and painful in their sockets. Visual
disturbances consisting of blurring, temporary blind-
ness, photophobia, and scotoma are common. Pupils
are usually dilated and the reflexes diminished. Skin
disorders are frequently reported that are usually
initiated by an intense generalized pruritus, accom-
panied by erythema, and maculopapular eruptions,
blisters, extensive areas of desquamation particu-
larly of the hands and feet and occasionally ulcera-
tion. There may also be a loss of hair and nails.

In severe intoxications the neurotoxic com-
ponents are especially pronounced. Paresthesias in-
volve the extremities, and paradoxical sensory dis-
turbances maybe present in which the victim interprets
cold as a "tingling, burning, dry-ice or electric-shock
sensation", or hot objects may give a feeling of cold.
In regard to the paradoxical sensory disturbance (P.
S. D. ), a classic example is that of a naval officer who
was poisoned by an amberjack. Four weeks later he


-11-








was observed subconsciously blowing on his ice cream,
which was "burning his tongue", in order to cool it.
Ataxis and generalized motor incoordination may be-
come progressively worse. The reflexes may be di-
minished, muscular paralyses may develop, accom--
panied by clonic and tonic convulsions, muscular
twitchings, tremors, dysphonia, dysphagia, coma, and
death by respiratory paralysis. The limited morbidity
statistics show a case fatality rate of about 12 percent.
Death may occur within 10 minutes, but generally re-
quire several days. "


Table 1 summarizes the symptoms occurring during the first 24

hours after ingestion as they were reported by 25 persons who

were interviewed following ciguatoxications of minor to moderate

severity in St. Thomas U.S. V.I. during 1971. Several of

these reports represent the symptoms produced in different

individuals by a single fish; they therefore do not represent 25

separate outbreaks.


TABLE 1. Summary of Symptoms


Symptom
abdominal pain
nausea
vomiting
diarrhea
numbness, tingling about mouth
headache
numbness in extremeties
metallic taste
weakness
muscle aches
paradoxical sensory disturbance
itching


Percent Reporting
96 (96)
88 (92)
68 (68)
96 (96)
56 (64)
48 (48)
48 (56)
24 (36)
96 (96)
40 (48)
32 (32)
64 (68)


Summary of symptoms manifested by 25 ciguatoxicated indi-
viduals during first 24 hours after ingestion of fish. (Percent-
ages in parentheses represent change in original descriptions
following questions by the interviewer.)


-12-









Several additional symptoms were reported by three

or fewer (less than 12%) of the persons interviewed. These

symptoms include lack of coordination, muscle spasm, high

fever, visual disturbance s, diminished reflexes, and skin

rash. It is notable that none of these persons required hos-

pitalization and only three reported visiting a physician (several

others contacted a p physician by telephone during the time

period 24 72 hours after ingestion).


Virtually all of the persons interviewed reported no-

ticeable symptoms of ciguatoxication for several days after

the onset of the incident. Most commonly reported was ex-

treme weakness and lethargy lasting up to two weeks. Many

victims reported gastrointestinal symptoms well into the third

day along with itching and/or skin rash. Those persons report-

ing the paradoxical sensory disturbance stated that it persisted

for at least three days, in some cases ten days or two weeks.

The bulk of the other symptoms noted were reported as having

dissipated within the first 24 hours.


We are currently undertaking a more extensive epi-

demiology reporting program in cooperation with local media,

physicians, and public health authorities. Data from this sur-

vey combining questionnaire and interview procedures should


- 13-









be available early in 1972. At this time we have no accurate

estimate of the magnitude of the ciguatera poisoning problem

in the Virgin Islands or for that matter anywhere in the eastern

Caribbean. Outbreaks in Puerto Rico are sufficiently notable

to receive coverage in the major English-language media which

suggests that they are infrequent. The officials responsible

for public health record-keeping in St. Thomas, on the other

hand, estimate three or four cases per week are seen in the

emergency room; if our 25 cases reported in table 1 represent

typical reporting ratios there may be as many as 30 cases per

week in St. Thomas. These figures probably represent the

maxima however and cannot be confirmed. Reports of cigua-

toxication in the British Virgin Islands have stated that virtually

"everybody" has been poisoned at least once (some as many as

fifteen times) but medical advice is almost never sought.

Interestingly the British Virgin Islands are the only demo-

graphic unit mentioned by Halstead (1970) where fish poisoning is

"not regarded as deterrent to the development of the fisheries

programme".


The pattern of sporadic reporting of ciguatera poi-

soning despite the relatively high incidence of the disease is

common throughout the northern Leeward Islands. Information


-14-









from Halstead (1970) and our own contacts with fishermen, in-

ter -island traders, charterboat operators and fishery personnel

in the region suggests that the problem is indeed severe. Vir-

tually every person contacted from St. Kitts, St. Maarten, St.

Eustatius, Anguilla, and Montserrat had either been a victim

himself or knew of a close friend or relative

who had been poisoned within the last five years. Very few

of these cases were brought to the attention of a physician;

most public health officials believe that "only the

very severe cases are brought to the attention of the medical

authorities" (Antigua); Halstead,(1970). One long-time resident

of St. Kitts estimates only about one case in ten receives

medical attention; as might be expected the bulk of the cases

reported involve tourists and non-native residents.


-15-










IV. GEOGRAPHIC DISTRIBUTION


The geographic distribution of ciguatoxic fish in the

Virgin Islands is shown in Figure 1. The island of St. Croix,

on a separate geologic platform, is not reported as producing

ciguatoxic fish in any appreciable quantity and has been omitted

from this figure. A large number of the areas indicated have

been reported as producing toxic fish for centuries. It cannot

be presumed that these are the only localities; toxic fish are

frequently caught in other areas.


In the Virgin Islands there is an extremely strong

feeling among the fishermen that the south side of the Virgin

Bank from Sail Rock east to Peter Island consistently pro-

duces toxic fish. Other fishermen would extend this area east

and north to include most of the coastline of Virgin Gorda,

some would include the Horseshoe Reef and Anegada. Still others

(particularly those who regularly fish this southern Bank) state

that only specific locations in this area produce toxic fish and

that reef areas or "banks" only a few miles away are free

of ciguatera. Virtually all fishermen feel that the entire north

side (the Atlantic side) of the Bank is free of toxicity with the

exception of a very few species. This pattern of geographic


-16-















100 fathn r


/

/


-'.
1




.-

e ..

I.


- .


* -.


Guana(

Jost
TS STrwe


9



Salt .-
-.4r


. itoo fathm.


a Norman


Buck '
/l
OFrenchcap /-B



100 fathcus


FIGURE 1
Map of the Virgin Islands area

-----* 100 fathoms curve
a areas reported as producing
toxic fish


Horsedxs
Reef








distribution of ciguaioxic fishes seems consistent with those

areas reported by earlier authors (Walker, 1922; Arcisz, 1950;

Brown, 1945; de Sylva, 1956, Mann, 1938). Other writers

quoted in Halstead (1967) notably Hill (1868) Rogers (1899) and

Gilman (1942), are contradicted by local fishermen, at least for

the bulk of the species implicated elsewhere in the Virgin Is-

lands.


In almost all reports on the geographic locality where

toxic fish are caught the interviewee was referring to depths

of 30 fathoms or less; the bulk of reports refer to reef areas

in eight fifteen fathoms, but this may be an artifact of fishing

methods rather than biological distribution. The relationship

of depth to capture of ciguatoxic fishes is discussed in a later

section.


The areas reported (by our contacts and by Halstead,

1970) as producing toxic fish in the northern Leeward Islands

are shown in Figure 2. These data are plotted along with areas

mentioned as toxic by various authors in Halstead (1967) and

do not represent an intensive survey. More .specific data will

be presented in a later paper. The more southerly group of

islands in the eastern Caribbean (Martinique south to Trinidad:

the Windward Islands) have not commonly been reported as pro-

ducing ciguatoxic fish in this century. Earlier authors make

-18-










reference to a variety of species and locations but this is not

confirmed by present residents.


Although no quantitative data are available it seems

clear that the majority of ciguatera poisoning outbreaks in the

eastern Caribbean occur in a rather small area from Mont-

serrat north to the Virgin Islands including all of the northern

Leeward Islands and portions of Saba and Anguilla Banks. Be-

yond this area ciguatera poisoning is limited to sporadic out-

breaks which generally involve large specimens of only a few

species.


-19-













FIGURE .2
Map of the Leeward Islands

--- 100 fathoms curve
a areas reported as
producing toxic fish


r '!
1' ~
9*~*~* 9
A


4~ A~*\
--A


-. Anguilla Bank
a'-'' .. -

^., r^ An~guilla





--St. Maarten
'-. ^^ 7 t'tMarten


'-I


/
/'
.'


I


lb
lb.


,\ ;,V St. Baits


I

p.' -
'P..


Saba Bank
I
.V

19
a/
* - *


I '.' -.\
'-,^St. Eustatius


N,


St. Kitts


. I Nevis






*t.*


Mmntserrat


PAGE 20


\. 'p
'>./'


.4


C "-" *
4-


I--
gsaba


/
-S
.- "p.
A


BarbIa
Bazbuxfa W "


/




a.
I

* 4.


* /1


a.,_


.
-''


/



I
i Antigua




i -
.
a'
V
'4. _I


-- *",





* a
'a'"









V. SPECIES REPORTED AS CIGUATOXIC


More than 400 species of fish have been implicated in

ciguaterapoisoning on a global basis (Bagnis, 1970). Of these

400, 91 species could conceivably be found in the eastern Ca-

ribbean. It is possible that an -even larger number could be

associated with ciguatoxications if they were desirable as food

fish. There are also a number of reports of molluscs, crabs,

and lobsters producing the disease. Appendix I lists the 24

fish most frequently reported as toxic in the Virgin Islands.

All of these species are valued as food fish with the exception

of barracuda and amberjack; these two species have such a

bad reputation as ciguateric that only the smallest specimens

can be sold. It is somewhat surprising that the moray eel is

as highly esteemed as it is, considering reports of toxicity

from the Pacific. In St. Thomas eels are typically purchased

by individuals from Spanish Caribbean cultures (Puerto Rico,

Dominican Republic, Cuba), areas where ci gu at e r a is less

frequently reported. The fish at the top of the list tend to be

reported as toxic more frequently than those lower down.


In general the larger specimens of these species are

frequently incriminated in ciguatera poisoning incidents. The

fish generally can be considered "shor e-fi she s" or "reef -

-21-










fishes" and for the most part conform to the pattern noted by

other authors (Randall, 1958; Halstead, 1967; Banner, 1971):

toxic fishes are not common at depths greater than 80 100

fathoms. Two notable exceptions in the Virgin Islands are the

blackfin snapper, Lutjanus buccanella and misty grouper,

Epinephalus mystacinus. We have data on two outbreaks af-

fecting five people from blackfin snapper caught in deep water

and three additional outbreaks implicating misty grouper (which

has not been taken at depths of less than 55 fathoms) involving

at least ten persons during mid-1971. These data appear in

Appendix II. Additional data on ciguatera from deep-living

species is noted in a later section of this report. Although

Banner (1971) states "true ciguateric fishes appear to be only

those fishes tied directly to the flora and fauna of coral reef.. "

there is excellent clinical data to support these outbreak re-

ports; several members of our staff were among the victims.

Samples have been retained for extraction and bioassay to

quantify the toxicity of .these fish (see also section on fisheries

development).


-22-









VI. CHEMISTRY AND PHARMACOLOGY


Our knowledge of ciguatera poisoning in the eastern

Caribbean is presently based upon clinical reports and is only

beginning to be quantified by chemical and biological assays.

On the basis of symptomology and from the species implicated

it is highly probable that ciguatera poisoning in the eastern

Caribbean is produced by very similar (if not identical) com-

pounds to those known from the Pacific. Scheuer and other

workers at the University of Hawaii have isolated what they

consider to be the primary toxin and, in cooperation with

Hashimoto and his colleagues at the University of Tokyo;

several secondary toxins. The primary toxin (deemed cigua-

toxin) is insoluable in water, soluable in polar organic sol-

vents, heat stable to 1000C, stable below 0C as a crude toxin

but unstable in the semipurified or purified form unless ex-

tracted, purified, and stored in an inert atmosphere at low

temperatures. The non-crystalline product has the empirical

formula (C35H65NO3)n and the molecule has indications of a

quaternary nitrogen atom, one or more hydroxyl groups and a

carbonyl function. It is not a phospholipid. A c-r ystalline

product currently undergoing analysis to determine its structure -

al formula (Banner 1971).


-23-









Present evidence (again from the University of Hawaii

group) suggests that ciguatoxin acts upon excitable membranes

to increase the permeability of Na + ions, upsetting the ionic

balance of the membrane. Ciguatoxin is not an anticholinesterase

in vivo, despite earlier papers and various therapies for cigua -

toxications based on stimulation of cholinesterase cannot be

endorsed at the present time. The toxin is active at the level

of 0. 025 mg/kg when injected into mice with a toxin yield of

5 10 mg/kg from highly toxic flesh. The toxin is carried at

a uniform level throughout the musculature of toxic fish but

may be 50 to 100 times as concentrated in the viscera, par-

ticularly the liver.


Our laboratory in St. Thomas is currently using an

acetone diethyl ether extraction with purification by column

chromatography developed by Scheuer (per. comm.) and bio-

assay using intraperitoneal injection into 20+ gram Charles

River CD-1 mice. We have previously used other extraction

techniques including crude aqueous extraction with emulsifiers

and a variety of experimental bioassay techniques. Our con-

clusions are basically the same as the workers in Hawaii al-

though based on much less experience: careful solvent ex -

traction and purification are necessary, rigidly cont r oled

bioassay procedures are required, and experienced laboratory

-94-









personnel are an absolute requirement. To date there has

been no rapid, simple colorimetric or other chemical test for

ciguatoxin developed. Screening programs are exceedingly ex-

pensive and difficult to manage and are only in operation in

Japan on a limited basis for s e 1 e c t e d samples from highly

suspect areas. As much as we might desire it, we are not

very close to a rapid means of identifying ciguatoxic fish in

the laboratory and even further from a simple test which might

be part of a housewife's shopping kit.


The traditional West Indian methods of determining if

a fish is ciguatoxic have been discussed at length by previous

authors. Appendix III lists these methods as reported to us by

natives of the Virgin and Leeward Islands. Many housewives

swear by some particular method utilizing visual inspection of

external characters of the fish. Most admit that in practice

both the visual methods and those requiring addition of some

indicator are unreliable. We have submitted each of these

methods to an assay with at least two known toxic fish and two

non-toxic fish and have not found them reliable.


-25-








VII, BIOGENESIS AND TRANSMISSION OF CIGUATOXIN


At the present time ,we have no accurate data on the

mechanisms of biogenesis of ciguatoxin (or its related compounds)

nor information on its transmission through the food chain.

Banner, Helfrich, Randall, and others at the University of

Hawaii have concentrated a good deal of effort on these prob -

lems in the Pacific and their findings to date are summarized

below (from Banner, 1971):


1. No causative agent or organism has yet been

identified as producing toxins similar to ciguatoxin.

2. No definite evidence has been found to suggest

that: a) copper or other metallic ions act as chelators, trace

minerals or catalysts in the formation of the toxin; b) no

demonstrable increase in ciguateric fishes was noted in areas

where new surfaces were exposed by natural disasters,

dredging, blasting, predation by Acanthaster; c) contamination

of the marine environment by pollutants (specifically wax esters

at Wake Island) have no effect on ciguatera.

3. Normally non-toxic omnivor es can be made

toxic when fed small amounts of toxic fish over a period of

time.


-26-









4. Toxic Lutjanus bohar retain toxicity for up to

30 months when fed a non-toxic diet.

5. A detrital feeding acanthurid ( Ctenochaetus

striatus) has demonstrable ciguatoxin in the flesh, viscera,

and gut contents.

6. Most carnivores seem to carry the same toxin

(ciguatoxin) although additional toxins (eg: Aluterin, ciguaterin)

may also be present.


It should be noted that Dr. Banner will present a paper entitled

"Biological Origin and Transmission of Ciguatoxin" tomorrow

(18 November 1971), which could shed some new light on this

subject.


Given the similar symptoms and species distribution

reported in Pacific and eastern Caribbean ciguatera poisonings

it is reasonable to assume that similar biogenesis and trans-

mission of the toxin can be expected. There are several per-

sistent beliefs among eastern Caribbean fishermen which will

be repeated here although we have beenunable to confirm them.


1. Ciguatera is produced by fish which eat the fruit

or leaves of manchineel (Hippomane mancinella). This theory

has been proposed since 1511 (by Peter Martyr of Anghera;


-27-










Halstead, 1967) and is probably based on advise to early ex-

plorers from Caribbean Indians. Hippomane is certainly toxic

but its pharmacological action is quite different. It is doubtful

that this theory is correct.

2. The most persistent theory in the Vi r gin and

Leeward Islands involves copper. Natural copper deposits

("copper banks") are presumed to exist and fish which feed on

these banks become toxic. Some of the more sophisticated

fishermen suggest that it is not actually the copper metal but a

small "sea moss" (which grown in areas where copper con-

centrations are high) which actually manufactures the toxin or

a precursor. The "sea moss" responsible has been pointed

out to us by several fishermen (actually) three species:

Enteromorphialingulata from shallow water at Buck Island, St.

Thomas; Cladophora sp. from fish pot warps of Flanagan Is-

land, U. S. V. I.; Chaetomorphia sp. from rocky s u b t i d a 1 at

Buck Island, St. Thomas). None of these algae showed toxic

activity when extracted with Tween and injected I. P. into mice;

we plan to repeat this experiment with solvent solvent ex-

traction and column chromatography when these algae can be

collected from historically toxic areas. Most fishermen

suggest that the production of toxic "sea moss" is seasonal


-28-









with peak growth in late spring or early summer. The asso-

ciation of ciguatoxin with copper is not limited to copper banks

by fishermen; it is proposed that shipwrecks (particularly older

wrecks with copper-sheathed bottoms) and copper antifouling

paints supply all of the copper needed. We can in no way con-

firm the theory of copper-induced ciguatoxin at this time.

3. A theory proposed by a few fishermen and com-

pletely unproven at this time attempts to explain the high con-

centrations of toxic fish on the south of the Virgin Bank (with

the lower toxicity reported from the same species on the north

side of the Bank) and in the area from Antigua north to the

Anegada Passage. It is proposed that the toxin is produced by

some organism (presumably a primary producer) which is found

only in areas where deep, cold, nutrient-laden water is upwelling.

The theory is reasonable when applied to the southern Virgin

Bank and the southeastern portions of Saba Bank, both noted as

producing toxic fish, as there is good evidence that upwelling

does indeed occur in the Anegada Passage. The upwelling pro-

cess cannot be confirmed in the St. Kitts St. Eustatius -

Redondo area at the present time due to lack of data. The

specific organisms(s) responsible and the mechanism of toxin

production are not known by the proponents of this theory.


-29-









We are therefore no closer to an accurate description

of the biogenesis or transmission mechanisms of ciguatoxin than

purely theoretical considerations. We have proposed a series

of studies similar to those undertaken by the Univer sity of

Hawaii group including chemical, ecological, and epidemiological

programs for the next three years to attempt a better under-

standing of this problem.









VIII. EFFECTS OF CIGUATERA POISONING ON
THE DEVELOPMENT OF FISHERIES



We have every reason to believe that ciguatera poisoning

is a major impediment to the sale of local finfish in the Virgin

Islands and thus is a strong deterrent to expansion of the com-

mercial fisheries. Interviews by Halstead (1970) suggest that

this is true throughout the Leeward Islands too, although residents

of Antigua, St. Kitts, and St. Maarteo express the opinion that

there is little alternative to continued buying of local fish and

risk of intoxication.


InDammann's 1967-68 survey of commercial fisheries

of the Virgin Islands slightly more than half of total finfish con-

sumption was from local (U.S. and British V.I.) sources

(1, 672,400 of 3, 084, 373). We have no data on how much of the

fish imports could be replaced by local production if ciguatera

were not a problem. Interviews with fishermen suggest that

very few hotels and restaurants catering to the tourist trade

would purchase locally caught grouper, snapper, jacks, and

kingfish because of fear of fish poisoning. Dammann's Table 9

"Fisherman-reported problems in the Virgin Islands commercial

fishery" does not include any data on this subject, however Table

12 indicates that only two percent (two of 79) of the fishermen


-31-









contacted felt that there were "no fish" (commonly reported as

ciguatoxic) so one might assume that ciguatera was indeed con-

sidered a problem.


Two investigations of fisheries development potential

in the Virgin Islands area have recently been completed. The

first (Dammann et al., 1970) developed lines of approach carried

out in the second project (Brownell and Rainey, 1971) for ex-

panding the Virgin Islands fisheries through exploitation of deep

water stocks. This effort was motivated by several natural

limiting factors on the shallow water fish populations, among

them the risk of ciguatera poisoning. It now appears that even

species previously considered non-toxic because their normal

depth-range is greater than 100 fathoms are implicated in

ciguatoxications. Brownell and Rainey (1971) report three out-

breaks from mity grouper Epinephelus mystacinus taken at

130-135 fathoms and the only documented case of c iguat era

from a silk snapper Lutjanus vivanus from 110 fathoms. Two

questionable outbreaks are reported by Dammann et al. (1970)

from Epinephelus nigri tus (actually E. mystacinus). In addition

to the outbreaks reported for E. mystacinus and Lutjanus

buccanella in Appendix II, we are aware of several outbreaks

from L. buccanella attributed to fish caught during the exploratory


-32-










fishing projects of the UN/FAO Caribbean Fisheries Development

Programme (CFDP)in 1970 and 71. We are currently extracting

and bioassaying about two tons of fish caught on UN/FAO cruises

from areas where toxicity is reported. These data will be re-

ported in early 1972. Although these data will provide us with a

more precise estimate of the proportion of ciguatoxic fishes in

the deep shelf shelf-slope-populations, we have already

ascertained that this resource is not free of ciguatoxin.


The toxic blackfin snappers caught by the CFDP came

from Saba and Anguilla Banks; fishermen in Montserrat report

that most known poisonous fish had been captured in deep water

- up to 250 fathoms. It is highly probable that the abrupt drop-

off to depths of 200 fathoms or more surrounding many of the

Leeward Islands harbor excellent stocks of food fish but it is

quite likely that some of these species carry ciguatera poisoning.


Halstead's 1970 survey found that fishermen, fisheries

officers, and public health officials were almost unanimous that

ciguatera was a deterrent to de velopment of the commercial

fisheries. Most Islands reported ciguatera in fish from depths

of 0-60 fathoms and the most frequently toxic are all among the

first ten species listed in Appendix I. At least two large com-

mercial fishing operations in St. Maarten have given up shallow


-33-










water fishing because of repeated ciguatoxications by their catch;

several fishermen have reported having to discard large catches

of jacks and grouper because their previous catches had caused

poisoning. In the small communities of the Virgin and Leeward

Islands an individual fishermen is occasionally completely boy-

cotted because of his reputation for regularly landing toxic fish.

Fishermen are expected to be able to determine whether or not

a particular fish is toxic; an occasional instance is accepted,

however.


The fisheries of the Virgin and Leeward Islands do not

lend themselves to exploitation by large vessels with modern

ground fishing gear. The pelagic stocks are apparently not

sufficient to support a much larger fishing effort than is currently

in progress. There are probably not sufficient stocks in the

shelf-edge populations to withstand intensive fishing pressure

equivalent to the Gulf of Mexico Florida Straits snapper in-

dustry. The majority of fishermen in the eastern Caribbean are

owner-operators of small boats (20 feet or less) who rarely go

more than ten miles from their home port. These fishermen

could be trained and proper gear could be utilized for exploiting

the area's natural stocks both in shallow and deep water but fish

poisoning cases would be likely to increase. A thorough under-


-34-











standing of the ciguatera problem must be developed before ex-

pansion of the fi shery can be effectively accomplished.


-35-










IX. SUMMARY AND CONCLUSIONS


1. Fish poisoning in the eastern Caribbean is reported

from all of the islands of the northern Virgin and Leeward Islands

group. Puerto Rico, Hispaniola and St. Croix have a much lower

incidence rate as do the Windward Islands (Trinidad to Martinique).

2. Although c 1 u p e oi d, elasmobranch, tetraodontoid,

and hallucinatory fish poisoning are reported from the eastern

Caribbean, scombroid poisoning and ciguatera poisoning are con-

sidered to be most important. Because scombroid poisoning can

be prevented bymodern preservationtechniques and treatment of

the disease is specific and effective, it is considered a less se-

vere problem than ciguatera poisoning.

3. Epidemiological reporting of ciguatoxications has

only been begun in the last month throughout the Virgin Islands

and a careful survey of the Leeward Islands must await additional

funding. Ciguatera is presently reported as a severe public health

problem with only a fraction of the cases reaching medical atten-

tion. The problem seems most severe in the area from Mont-

serrat north to the British Virgin Islands including the south-

east portion of Saba Bank and the southern shelf of the Virgin Is-

lands pl at; au.


-36-









4. The chemistry, pharmacology, and ecology of

ciguatoxin and closely allied compounds are at present poorly

understood. The symptomology and species distribution of the

toxins in the eastern Caribbean strongly suggest that a situation

exists which is very similar to that described from the Pacific

islands by the Marine Biotoxin group at the University of Hawaii

over the past sixteen years.

5. Toxicity in eastern Caribbean fishes seems to be

more prevalent among the large carnivores of reef or reef-re-

lated habitats. There are a number of data which suggest that

ciguatoxin(s) are produced by some organism in the reef food web

and that the toxin is passed through the food web without a signi-

ficant modification and concentrated by the larger carnivores.

6. Development of the commercial fisheries in the

eastern Caribbean is severely impeded by the prevalence of

ciguatoxin in commercially desirable species. There is good

evidence that the shelf-edge stocks of snapper and grouper are

not free from ciguatera poisoning as previously proposed and

that exploitation of this presently underutilized resource may be

impeded by this toxicity.


3-7 -









X. ACKNOWLEDGEMENTS


This report was prepared with the cooperation of the

staff of the Ciguatera Project, Caribbean Research Institute,

College of the Virgin Islands. The Ciguatera Project is supported

by a Sea Grant (1-35368) from the National Oceanic and Atmospheric

Agency of the U. S. Department of Commerce with matching con-

tributions from the United Nations Food and Agriculture Agency's

Caribbean Fisheries Development Programme, the College of the

Virgin Islands, and the G o ve rnment of the U. S. Virgin Islands.


-38-









XI. LITERATURE CITED


Arcisz. W. 1950. U. S. Fish & Wildlife Serv. Sp. Sci. Rep. no.
27, 1-27

Bagnis, R. et al. 1970. Bull. World Health Org. 42:69-88.

Banner, A. H. 1971. Tech. Report #1 (Final Report) ONR
Contract #N00014-67-C-0127.

Brown H. H. 1945. Develop: Welfare West Indies, Bull. 20:
34-37

Brownell. W. N. & W. E. Rainey 1971. Carib. Res. Inst. Rept.
VIERS no. 3.

Dammann, A. E., W. Swingle & J. Yntema 1969. Carib. Res.
Inst. Spec. Rept. VIERS no. 1

et al. 1970. Carib. Res. Inst. Spec. Rept. VIERS
no. 2.

de Sylva, D. 1956. Mar. Lab. Univ. Miami. Spec. Serv. Bull.,
v. 13:1-9.

Gilman, C. L. 1942. U. S. Nay. Med. Bull. 40(l):19-27.

Halstead, B. W. 1967. Poisonous and Venomous Marine Animals
U. S. G. P. O.

1970. UN/FAO CFDP working paper FI:SF/CAR Reg.
189.

Hill, R. 1868. Proc. Sci. Assoc. Trinidad 1 (5)210-223.

Mann, W. L. 1938. U. S. Nay. Med. Bull. 36(4):631-634.

Randall, J. E. 1958. Bull. Mar. Sci. Gulf Caribbean 8(3):236-267.

Rogers. J. M. 1899. Pop. Sci. Monthly 55:680-685.

Teytaud, A.R. & R.W. Brody 1971. Carib. Res. Inst. Spec. Pub.
Cig. no. 1.

Walker, F.D. 1922. U.S. Nay. Med. Bull. 17(2):193-202.

-39-








APPENDIX I


Species Most Commonly Reported as Toxic in the Virgin Islands
Area


Species

Sphyraena barracuda
Seriola dumerili
Caranx latus
Caranx ruber
Caranx hippos
Lutjanus jocu
Mycteroperca venemosa
Scomberomorus cavalla
Caranx fusus
Gymnothorax funebris

Epinephelus adscensionis
Mycteroperca bonaci
Scomberomorus vegalis

Caranx lugubris
Lutjanus griseus
Lutjanus buccanella
Epinephelus mystacinus

Epinephelus guttatus
Seriola rivoliana
Caranx bartholomaei
Apsilus dentatus
Epinephelus morio
Lachinolaimus maximus
Belistes vetula


Common Name

Great barracuda; barra
Amberjack; amber
Horse-eye jack
Bar jack; carang
Crevalle jack
Dog Snapper; dog tooth
Yellowfin grouper; gramminix
Kingfish; king mackerel
Blue runner; hard nose
Green moray (probably Conger
or Congo eel)
Rock hind
Black grouper
Cero (often mistaken for
"spanish mackerel")
Black jack
Grey snapper
Blackfin snapper
Misty grouper (often erroneously
called Warsaw grouper)
Red hind
Almaco jack
Yellow jack
Black snapper
Red grouper
Hogfish
Queen triggerfish; old wife










APPENDIX II

Outbreak reports from fishes caught at depths greater than 500
feet during 1970-71 (data from interviews; Ciguater a Case
Repository numbers refer to CRI files)


CCR-71-011. Blackfin snapper Lutjanus buccanella about
four lbs. Fish caught south of Frenchcap Cay, U. S. V. I.
at about 40 fathoms bylocal fishermen. Fishwas eaten
by three people all of whom reported abdominal pain,
bowels, nausea, vomiting in that order. Onset between
three and six hours after ingestion. Secondary symptoms
included extreme weakness, listlessness, itching which
developed 12-24 hours after ingestion and lasted for
several five seven days. None of the victims reported
previous intoxication.

CCR-71-018. Blackfin snapper Lutjanus buccanella about
three lbs. Fish was purchased on the waterfront at St.
Thomas by young couple visiting relatives on the island.
Fish was broiled with sauce, no symptoms developed
until about eight hours after ingestion. Vomiting, diar-
rhea, weakness in the knees, dull headache persisted all
the following day. Late afternoon produced P. S. D. for
man but not wife. Returned to mainland three days after
ingestion, no followup available.

CCR-71-008. Misty grouper Epinephelus mystacinus 36
lbs. Fish purchased at the dock caught (apparently)
south of St. John. Victims brought five lbs. (tw, large
steaks); refrigerated them and cooked fish next evening.
Four persons had dinner of this fish; three young men
and a young lady one man and the lady reported nausea,
vomiting, and weakness within six hours; headache,
nausea, weakness persisted for "three or four days".
The third victim had no violent symptoms of gastro-
intestinal origin but was lethargic and felt "weak in the
joints" next day. The fourth person did not report any
illness.











CCR-71-021. Misty grouper Epinephelus mystacinus 56
lbs. Fish caught bylocal sport-commercial fishermen
at the "Warsaw Pocket" (misnamed since the area pro-
duce misty groupers) about 3-1/2 miles south of Nor-
man Island, B. V. I. at depth of about 120 fathoms. Fish
was filleted and headed; at least six persons ate fillets
with no ill effects. Two more people made soup of the
head; they reported some intestinal discomfort and weak-
ness, tingling sensations and lethargy the following day.
Five other persons fried a small section of the liver:
each reported eating "not more than a few bites" that
night. All awoke within three hours with violent abdominal
cramps, vomiting, and violent headache.
Severity of gastrointestinal symptoms continued for six
hours or so, then extreme '.'.akness, sinus-like head-
ache, and watery bowels persisted for two four days.
P. S. D. and tingling and numbness in the lips were re-
ported about sixteen hours after ingestion by three of the
five. All reported persistent symptoms of weakness and
soreness in all body joints for seven ten days. P. S. D.
persisted for at least a week in two victims.

CCR-71-023. Misty grouper Epinephelus mystacinus a-
bout 30 lbs. Steaks were sold to about four persons
none of who apparently developed ciguatera symptoms.
A soup was made of the head and eaten by three persons.
All described gastrointestinal distress, diarrhea, and
nausea within three six hours; apparently the symptoms
disappeared within about 24 hours for two of the victims;
the third reported listlessness, weakness, and achy
joints which lessened by the third day after ingestion.









APPENDIX III


Methods for identifying ciguatoxic fish as described in the folk-
lore of the Virgin and Leeward Islands (from interviews; Dam-
mann et al., 1969; Halstead, 1967)


I. External characters of the fish or fish flesh which indicate
toxicity:

-More yellow or brassy color, especially about the head
-Stripes (in species where they are not normally obvious)
-Darker coloration
-Red coloration to the eyes
-Yellow mucus on inner lining of gullet
-Green tint to raw flesh
-Tiny black "veins" running through the musculature
-Brassy or coppery odor to the flesh
-Teeth are black
-Suspect specifies with roe is toxic
-Enlarged or bloated stoifnach
-Flesh tastes bitter or hot in mouth

II. Indicator organisms which suggest toxicity:

-Worms in the flesh (particularly jacks and mackerel)
(Worms in the stomach indicate a non-toxic fish)
-Isopod ectoparasites ("cockroach") are not found on toxic
fish (jacks)
-Flies will not land on flesh
-Ants will not eat

III. Methods employing an indicator:

-Silver turns black when boiled with toxic fish
-Sweet potato turns black when boiled with toxic fish




University of Florida Home Page
© 2004 - 2010 University of Florida George A. Smathers Libraries.
All rights reserved.

Acceptable Use, Copyright, and Disclaimer Statement
Last updated October 10, 2010 - - mvs