Journal of Plankton Research Vol.14 no.11 pp.1581-1592, 1992
Occurrence of dinoflagellate Alexandrium tamarense, a causative
organism of paralytic shellfish poisoning in Chinhae Bay, Korea
Myung-Soo Han 1 , Joong-Kyun Jeon and Young-Ok Kim1
Marine Biotechnology Laboratory, Korea Ocean Research and Development
Institute, Ansan, PO Box 29, Seoul 425-600, Korea
Abstract. A paralytic shellfish poisoning (PSP) incident caused by consumption of the mussel Mytilus
edulis occurred for the first time in Korea in April 1986. Weekly water samplings were carried out
during the period from 7 March to 21 April 1989 in Chinhae Bay, Korea, in order to identify the
causative organism. The temperature characteristics of the water column indicated three different
hydrological regimes: well mixed (up to 7 March), weakly stratified (17-31 March) and stratified (721 April). Toxicity of the phytoplankton was detected during the weakly stratified period, but only in
the 10-50 nm phytoplankton size fraction. This study presents the occurrence of the toxigenic
dinoflagellate Alexandrium tamarense, which is a causative organism of PSP, in Korean coastal
waters. Its biomass varied at different depths in the water column, ranging from 200 to 8000 cells I"1
in the water column. The weekly fluctuation of A.tamarense toxicity was similar to that of mussel
toxicity.
Introduction
Some species of dinoflagellates are known to be the causative organisms of
paralytic shellfish poisoning (PSP) and diarrhetic shellfish poisoning (DSP).
Among organisms causing PSP, Alexandrium tamarense is commonly present in
temperate waters (Anderson et al., 1985; Okaichi et al., 1989; Graneli et al.,
1990). In April 1986, a poisoning incident occurred for the first time near Pusan
(Gamrae-po) due to the consumption of the mussel, Mytilus edulis. The lethal
potency of shellfish extract (PSP) in mice reached 490 mouse units (MU) g"1
(Chang et al., 1987; Jeon et al., 1987). Since then, an extensive survey of the PSP
toxins in Korean shellfish has been actively pursued [Korea Ocean Research and
Development Institute (KORDI), 1988, 1989].
Semi-enclosed, Chinhae Bay is located in the southeastern part of Korea and
its water circulation is restricted because of its narrow mouth (Figure 1). Since
the 1970s, eutrophication in the inner part of Chinhae Bay has accelerated due
to fertilization with large inputs of domestic and industrial wastes (Lee et al.,
1981; Yoo and Lee, 1985; Park et al., 1989; Yang, 1989). In addition, many
shellfish culture farms have been established in and around this bay (Yang and
Hong, 1988). During the last decade, harmful algal blooms were frequently
observed in Chinhae Bay (Cho, 1979; Park et al., 1987). Causative organisms of
these algal blooms were dinoflagellates such as Ceratium fusus and
Gymnodinium nagasakiense. However, PSP toxigenic algal species had not yet
been reported, although three Alexandrium species were described (Lee, 1990)
and PSP had been detected from wild and cultured bivalves in Chinhae Bay
(Jeon et al., 1988; Chang, 1991). Our purpose here is to identify a PSP causative
© Oxford University Press
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' Present address: Department of Biology, College of Natural Sciences, Hanyang
University, Seoul 133-791, Korea
M.-S.Han, J.-K.Jeon and Y.-O.Kim
organism for paralytic shellfish toxins in mussels by collecting, identifying and
counting phytoplankton at weekly intervals. We document here, for the first
time, the occurrence of the toxic dinoflagellate, A.tamarense, in Korean coastal
waters.
Method
Results
Morphological characteristics and vertical distribution of A.tamarense
We found A.tamarense as a possible causative organism of PSP at all stations in
Chinhae Bay, Korea. Figure 2 shows the morphological characteristics of
A.tamarense. Cells are globular, usually slightly greater in length than in width.
Cells are solitary, but a chain of two cells is sometimes found (Figure 2a). The
first apical plate (1') with the ventral pore is connected with the triangular apical
pore plate (Po) (Figure 2b,d and f). A fish hook-shaped apical pore is located on
the left side of the apical pore plate, and the anterior attachment pore is sealed
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Water samples were collected weekly from five different depths at five stations
in Masan (Station M) and Chilchundo waters (Stations C1-C4) of Chinhae Bay
during the period from 7 March to 21 April 1989 (Figure 1). Phytoplankton
samples were preserved with 2% glutaraldehyde in 250 ml plastic bottles.
Phytoplankton species were identified and counted under a differential
interference microscope (Carl Zeiss, Axioskop). For detailed observations, a
scanning electron microscope (JEOL, JSM-35C) was used. Identification at the
species level was made on diatoms, dinoflagellates and other flagellates.
Morphological characteristics of the genus Alexandrium were confirmed by
dissecting thecal plates in 5% sodium hypochlorite solution.
Mussels, M.edulis, were obtained from four stations (M, Cl, C3 and C4) in
Masan and Chilchundo waters. The mussels were immediately frozen, transported to the laboratory and stored at — 30°C until analysis. Mussel toxicity was
assayed by the official method for PSP (Kawabata, 1978). Briefly, the edible
portion of mussel was homogenized in a mortar with a pestle, after adding 4 vols
of 0.1 N HC1, and the mixture was then heated in a boiling water bath for 5 min.
The combined supernatant was directly injected i.p. into a group of ddY strain
male mice (18-20 g). Lethal potency was calculated using the time required to
kill the mice and expressed in mouse units (MU). One MU is defined here as the
amount of toxin which kills a mouse within 15 min after i.p. injection.
Large volumes of surface seawater samples (20-50 1) were collected from all
stations and fractionated in four size classes of phytoplankton (<10, 10-50, 50100 and 100-300 u,m) with sieves. Fractionated subsamples were harvested on
Millipore membrane filters (0.2 |xm) and 2 vols of 0.1 N HC1 added. The
mixture was then sonicated and heated in a boiling water bath for 5 min, and
centrifuged at 2000 r.p.m. for 15 min. Each size fraction was tested for toxicity
by i.p. injection in the same manner as previously described. The toxicity of
phytoplankton size fractions is expressed per 20 1 of concentrates.
Alexandrium tamarensem Chinhae Bay, Korea
128*30'E
128 50
- 34*50'
Fig. 1. Sampling stations in Chinhae Bay, Korea.
(Figure 2c). The posterior attachment pore in the sulcal posterior plate is also
sealed (Figure 2e). Anterior and posterior attachment pores were not observed
despite detailed plate analysis of >200 natural cells. Schmidt and Loeblich
(1979) and Fukuyo et al. (1985) reported that posterior and anterior attachment
pores, in non-chain-forming cells of both culture medium and natural waters, are
sealed.
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35 1O'N
M.-S.Han, J.-K.Jeon and Y.-O.Kim
10 (Jim.
The vertical distribution of A.tamarense in Chinhae Bay is shown in Figure 3.
Alexandrium tamarense was found at densities ranging from 200 to 8000 cells I"1
during the period from 7 March to 21 April 1989. The biomass of the
dinoflagellate A.tamarense was particularly high in the middle layer and near the
bottom of the water column in the early part of the sampling period (before 31
March), just before the onset of water column stratification. Along with the
development of water column stratification due to a rise in water temperature,
the biomass of A.tamarense decreased significantly, even though A.tamarense
was again observed in the later period. Toxicity of A. tamarense was seen in the
early part of sampling period, but decreased significantly in the later period.
Water temperature
The thermal structure of the water column is shown in Figure 4. Water
temperature in Chinhae Bay varied from 8.2 to 15.0°C during the sampling
period. Water temperature showed similar temporal distributions at all stations.
The water column was vertically well mixed until 7 March and gradually
stratified thereafter. Three different water column conditions could be distinguished: well mixed (up to 7 March), weakly stratified (17-31 March) and
well stratified (7-21 April). However, the structure of the temperature at
Station Cl did not fit in this classification because tidal and wind-driven currents
passed rapidly around this area (Kim et al., 1989).
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Fig. 2. Morphological characteristics of A. tamarense. (a) ventral view (chain form); (b) epitheca; (c)
apical pore complex; (d) detail of the first apical plate showing ventral pore; (e) sulcal posterior plate
with sealed posterior attachment pore; (f) ventral view (scanning electron microscope): apical pore
complex and ventral pore are marked by upper and lower arrows, respectively. Each scale bar is
Alexandrium tamarense in Chinhae Bay, Korea
Alexandrium tamarense (cells/1)
o
400
2
Sta. M
4
7
10
0
TI53?
'
OCU;
500
Sta. C1
500
13
0
Sta. C2
3
500
13
o
Sta. C3
500
13
Sta. C4
00
2000
J
1000
13
f*\
19
7
Mar.
1989
17
25
31
7
Apr.
14
21
Date
Fig. 3. Vertical distribution of A.tamarense cells in Chinhae Bay, during the period 7 March-21
April 1989.
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V^~iooo-^ J
M.-S.Han, J.-K.Jeon and Y.-O.Kim
Water temperature (°c)
Sta. M
8.6
9.0
9.4
10 2
9.8
10
o
StaC1
8
8.2
13
0
9.0
9.4
9.8
12 2
10.2 10.6 1 1 0 '
-
13
° 13.4
Sta. C2
3
E
"5.
8
7.6
10.0 10.6
8.8
11.211-8
13
Sta. C3
13
0
7.8
Sta. C4
3
13
7.8
19
7
Mar.
1989
17
8.2
25
8.6909.49-8
31
10.6
7
Apt
14
21
Date
Fig. 4. Time series distribution of water temperature in Chinhae Bay in the period 7 March-21 April
1989.
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3
Alexandrium tamarense in Chinhae Bay, Korea
Toxicity of M.edulis
Toxicity of fractionated phytoplankton and A.tamarense
Toxicity of four different size fractions (<10, 10-50, 50-100 and 100-300 \im)
of surface phytoplankton at five stations is given in Table I. Toxicity was only
detected in the size range from 10 to 50 u.m during the period from 17 to 31
March when the water column was weakly stratified. The magnitude of toxicity
in the 10-50 n-m fraction varied from 0.7 (17 March, Station C4) to 3.2 MU per
20 1 (25 March, Station C4). These results suggest that toxins were contained in
the 10-50 (Am size fraction. The genus Alexandrium, which is known to produce
paralytic shellfish poisons (Needier, 1949; Prakash, 1963; Graneli et al., 1990),
ranges from 20 to 50 \i.m in length and 20 to 60 |xm in width (Fukuyo, 1985).
Therefore, attention was focused on studying a possible link between the toxicity
of the 10-50 \im size fraction and the occurrence of the genus Alexandrium.
Phytoplankton toxicity in the 10-50 n-m fraction was divided by the cell
numbers of A. tamarense. This value was used as an index of cellular toxicity for
A.tamarense. Cellular toxicity was not detected during the latter part of the
sampling period (Figure 5). Although only a little data on the toxicity of
A.tamarense was available, the trend was similar to that for mussel toxicity.
Toxicity of A.tamarense varied widely, from 2.7 (Station C4, 31 March) to
19.2 x 10~5 MU cell"1 (Station C3, 31 March). Toxicity of the dinoflagellate
was seen only in the early part of the sampling period, even though A. tamarense
was again observed at surface waters of station Cl and C4.
Discussion
Recently, the frequency, intensity and geographical distribution of toxic
plankton blooms appear to be increasing (Granmo et al., 1988; Hallegraeff et al.,
1988). Until recently, toxic plankton bloom had not been known in Korean
coastal waters. However, in spring 1989, PSP contamination of wild mussels
coincided with blooms (5 x 105 cells I"1) of A.tamarense at Gamrae-po, near
Pusan, in the southern part of Korea (M.S.Han, unpublished data). Such a high
biomass has never been reported before in Korean coastal waters. The mussel
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The toxicity of bivalves in the Chinhae Bay waters has been investigated by
monthly samplings during 1987 to 1988 (Jeon et al., 1987, 1988). During the
survey, toxicity of M.edulis was detected mainly in spring. In other seasons, the
levels of toxicity were <2 MU g"1. Toxicity in M.edulis was detected continuously at all stations during the survey period (Figure 5). At Station M, mussel
toxicity reached up to 16 MU g"1 on 17 March 1989. The day after, it remained
<~4 MU g"1. At Station Cl, in the early period of sampling, mussel toxicity
was weak, while a higher toxicity of 21 MU g"1 was observed on 14 April. At
Station C3, toxicity of 23 MU g"1 was observed on 31 March. The highest value
in the survey area, 46 MU g"1, was recorded at Station C4 on 17 March.
Generally, mussel toxicity at the three sampling stations around Chilchundo was
higher than that at Station M during the survey period.
M.-S.Han, J.-K.Jeon and Y.-O.Kim
m
• M.edulis
O»»»o A. tamarense
40
Sta M
20
30
15
20
10
5
...••©
10
Sta.C1
5
40
20
30
15 S
20
10
CO
10
0
£
Sta.C3
"S 40
2
(0
C
CD
20
30
S
<
15 "S
20
10
2
.2
10
5
0
Sta.C4
0
40
20
30
15
20
10
10
5
0
0
17
25
31
7
Apr.
Mar.
1989
14
24
Date
Fig. 5. Toxicity of M.edulis and cellular toxicity of A.tamarense in Chinhae Bay in the period 7
March-21 April 1989.
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0
0
Akxandrium tamarense in Chinhae Bay, Korea
Table I. Toxicity of phytoplankton in the 10-50 p-m size fraction at the surface water in Chinhae Bay
(Stations M, C l , C2, C3 and C4) during the period 17 March-21 April 1989
Station
March
17
25
31
April
7
2.6
1.0
1.0
0.7
1.6
1.2
1.2
1.1
3.2
1.0
1.0
1.0
1.0
1.2
-
14
24
- : not detected.
digestive gland showed a lethal potency of 680 MU g ' of paralytic shellfish
poison. Its sudden mass occurrence in this area may be related to the
development of particular ecological conditions favorable for the growth of PSP
organisms such as A.tamarense (Hallegraeff et al., 1988).
However, we did not observe any higher cell density of A.tamarense nor PSP
toxicity in Chinhae Bay, near Pusan, in the same period. In fact, cysts of
A. tamarense in the surface sediments of Chinhae Bay were rare (KORDI, 1989).
This may explain why cell densities of A.tamarense were low in Chinhae Bay.
Nevertheless, cell numbers of A.tamarense increased temporarily in the early
period of sampling, during which the water mass was weakly stratified. In spring,
stratification of the water column gradually developed as a result of a rise in
water temperature with time. Dense populations of A.tamarense have been
mainly observed in stratified waters near the pycnocline in many localities
(Therriault et al., 1985; Cembella and Therriault, 1989). The density of the
environment, i.e. pycnocline, also plays an important role in the occurrence of
subsurface populations and has often been interpreted as an underlying factor in
phytoplankton patchiness (Rasmussen and Richardson, 1989). It is suggested
that subsurface populations of A.tamarense could be accumulated temporally
near the thermocline when A.tamarense are initiated through excystment from
benthic cyst populations, and growth of A.tamarense might be stimulated as
result of favorable hydrological conditions, such as a thermocline.
Cell numbers of A.tamarense decreased significantly in the later part of the
sampling period. There are two possible explanations: (i) increased temperature
and (ii) depletion of nutrients. After April, the growth of A. tamarense may be
limited as a result of a gradual rise (>15°C) in water temperature. Generally,
A.tamarense in the temperate zone is mainly distributed in cold waters of 7-15°C
(Fukuyo, 1982; Taylor, 1984). However this explanation seems unlikely because
the optimum temperature for this species was found to be 15-20°C in laboratory
experiments (Yentsch et al., 1975). Maclsaac et al. (1979) reported that the halfsaturation constant of nitrate and ammonium uptake for A.tamarense
(= Gonyaulax excavata) was similar to that of neritic diatoms and natural
phytoplankton populations from eutrophic regions. Depletion of ammonia and
phosphate was caused by a phytoplankton bloom during 17-25 March which had
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M
Cl
C2
C3
C4
Toxicity (MU per 20 I)
M.-S.Han, J.-K.Jeon and Y.-O.Kim
Acknowledgements
We are indebted to Prof. K.-I. Yoo, Hanyang University, and Dr H.T.Huh,
KORDI, for their helpful advice and encouragement, and to Prof. M.Takahashi
and Dr S.Taguchi for their critical discussions. We thank Mrs B.-H.Rho and
J.Yi for their cooperation in the field and laboratory. This study was supported
by the Ministry of Science and Technology of Korea (BSPG 00078-239-3).
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Downloaded from http://plankt.oxfordjournals.org/ at Penn State University (Paterno Lib) on May 16, 2016
Received on January 12, 1991; accepted on July 28, 1992