全 文 ：Received 10 Dec. 2003 Accepted 29 Jun. 2004
Supported by the State Key Basic Research and Development Plan of China (2001CB409702).
* Author for correspondence. Tel: +86 (0)592 2195338; E-mail: .
http://www.chineseplantscience.com
Acta Botanica Sinica
植 物 学 报 2004, 46 (9): 1025-1031
Cyst Formation, Development of Alexandrium tamarense from Yangtse
River Estuary and Its Relation to Bloom Dynamics
GU Hai-Feng1, 2*, LAN Dong-Zhao1, FANG Qi1, WANG Zong-Ling3
(1. The Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, China;
2. Ocean University of China, Qingdao 266003, China;
3. The First Institute of Oceanography, State Oceanic Administration, Qingdao 266011, China)
Abstract: The toxic dinoflagellate — Alexandrium tamarense (Lebour) Balech, formed resting cysts in
f/2 media with low nitrate concentrations. Among the concentrations tested, f/20 NO3- was the most
effective to induction with an encystment percentage of 2.0 in batch culture. About 73.2% and 17.6% of
cysts were produced on 8 and 9 d after transferring. Newly formed cysts developed accumulation body 3 d
later and kept forming mucilaginous substance, which might help their dispersal and survival. The manda-
tory dormancy period of resting cysts was 15 and 10 d when stored at 15 and 20 ℃ respectively. The cysts
could germinate without temperature change, with germination of 75.6% 20 d after formation at 20 ℃. The
Alexandrium cyst density in the surface sediment of DG-26 station reached above 25 cysts/g in May and
November of 2002, and dropped to 4.5 and 0.9 cysts/g in August of 2002 and February of 2003, suggesting
that Alexandrium cysts might have germinated in spring and autumn 2002. Cysts produced during the
bloom returned to water column soon, whatever the season and water temperature were. The cyst density
in the surface sediment at DG-26 station in May, 2003 was only 3.3 cysts/g and the cysts were newly
formed. In the Yangtse River estuary, the inoculum size was not a major factor to determine the outbreak
of A. tamarense bloom.
Key words: cyst; Alexandrium tamarense ; Yangtse River estuary; bloom
Alexandrium tamarense is one of the dinoflagellate spe-
cies responsible for harmful blooms and paralytic shellfish
poisoning (PSP) around the world (Hallegraeff, 1993). It is
also distributed widely in the Southern, Eastern and Yellow
Sea of China (Li and Xia, 1995; Gu et al., 2003). The resting
cyst (hypnozygote) is an important part during the life cycle
of A. tamarense, inhabiting the benthos when the environ-
ment is not suitable for asexual growth, and returning to
the water column later. The germination of A. tamarense
cysts provides the “seed population” for toxic bloom of
this species (Anderson and Wall, 1978; Anderson and
Morel, 1979; White and Hewis, 1982).
The mechanism of sexual induction in dinoflagellate re-
mains obscure. Wall (1970) hypothesized that sexuality was
not a reaction to adverse environment, but a natural phe-
nomenon in the dinoflagellate life cycle. Several field ob-
servation results have proved this (Anderson and Chisholm,
1983; Godhe et al., 2001). But in laboratory culture only a
few species can produce cysts in optimal environment
(Zingmark, 1970; Morey and Ruse, 1980), while most need
nutrient (N, P, Fe) depleted media for sexual induction
(Anderson, 1984; Doucette and Harrison, 1989; Olli and
Anderson, 2002). Cysts often have a mandatory dormancy
period in the sediment, which is the minimal time needed to
germinate from the time of formation. Cold temperature and
anoxia retard the germination of cysts, while other environ-
mental factors (nutrient, darkness, etc.) do not have obvi-
ous effects (Anderson, 1980). White (1982) reported that
empty cysts of A. tamarense began to appear in February,
although the water temperature was quite low at that time,
and accounted for 50% of the total in surface sediment
after June as the result of germination.
There have been large scale Alexandrium blooms in the
Yangtse River estuary in May of 2000 and 2002 with high
densities of around 5× 104 cells/mL (Wang and Huang,
2003), but we know little about life cycle transitions and the
role of cysts in bloom initiation and disappearance. We lay
emphasis on A. tamarense because more than 90% of the
ellipsoidal cysts from Yangtse River estuary produced this
species after germination. Others might be A. catenella.
The objectives of this report are to: investigate the encyst-
ment dynamics of A. tamarense from the Yangtse River
Acta Botanica Sinica 植物学报 Vol.46 No.9 20041026
estuary; clarify the maturation processes of cysts and un-
derstand the role of cysts in the bloom outbreak.
1 Materials and Methods
1.1 Samples
Sediment samples were collected from August, 2002 to
May, 2003 using a core sampler. Sediment treatment and
cyst enumeration were according to Gu et al. (2003). We
selected station DG-26 (122°3036 E, 29° 001 N) to study
the cyst dynamics since it had the greatest cyst density of
all stations in the Yangtse River estuary (Gu et al., 2003).
Water samples were collected from November, 2002 to May,
2003 and preserved in acid Lugol’s solution.
1.2 Cultures
Cultures of A. tamarense were established by incubat-
ing typical ellipsoidal cysts from sediment of Yangtse River
estuary (122°3036 E, 29°001 N) and nearby Weizhou Is-
land (109°2306 E, 21°012 N) in Guangxi Zhuang Autono-
mous Region. Cell morphology was examined under an
Olympus microscope. Cultures were maintained in f/2-Si
media at 20 ℃, 3 000 lx under 12:12 h light:dark cycle.
1.3 Encystment
Cells during mid-exponential growth were transferred to
12 well plates to yield an initial concentration of 120 cells/
mL. Preparation of encystment media and plates followed
the method of Anderson (1983). To examine the effect of
nitrate concentration on cyst formation, three media were
tested. They were f/2 media with nitrate reduced to 20%
(f/10 NO3-), 10% (f/20 NO3-) and 6.7% (f/30 NO3-) of f/2
level. To test short term induction effects on encystment,
nitrate was added to f/2 level on day 1, 2, 3, 6, and 9, with
the control kept at f/20 NO3- level. Cyst production was
calculated under an inverted microscope every day. All ex-
periments were maintained at least 15 d when the cyst num-
ber did not increase, and then total cells and cysts were
calculated.
1.4 Development of cysts
Newly-formed cysts were stored at 20, 15 ℃, 3 000 lx
under 12:12 h light:dark cycle. Cysts were examined for de-
velopment everyday and micropipetted to 96 well plates
filled with 100 mL f/2 media for periodical germination.
2 Results
2.1 Encystment
When the actively growing algae were transferred to
f/2 media depleted of N, they continued to grow in the first
several days. Fusing cells began to appear 1 or 2 d later.
The size of gametes was slightly smaller than normal cells
and there was no other obvious distinction between them.
The planozygote was deeply pigmented and larger than
normal cells, ranging from 47 to 52 mm long and 40 to 47 mm
wide (Fig.4). It had two posterior flagella and swam in the
water for several days before losing flagella and theca.
f/20 NO3- was the most efficient to induction media with
an encystment percentage of about 2.0, while f/10 NO3-
and f/30 NO3- was less efficient (Table 1). About 73.2% and
17.6% of cysts were produced on 8 and 9 d after transfer-
ring (Fig.1).
One or two days’ induction by f/20 NO3- resulted in an
encystment rate of 0.07, showing that it was possible for A.
tamarense to produce cysts after short-term induction.
When the induction time increased to 3 d or more, the en-
cystment rate did not show obvious difference to that of
control (Table 2).
Table 1 Culture media effect on cell yield (103 cells/ mL), cyst
yield (cysts/mL) and encystment percentage of Alexandrium
tamarense
Cell yield* Cyst yield* Encystment
(SE) (SE) percentage (SE)
f/2 3.84 (0.42) 0.00 (0.00) 0.00 (0.00)
f/10 NO3- 4.00 (0.61) 51.47 (18.31) 1.26 (0.26)
f/20 NO3- 3.26 (0.10) 65.07 (1.89) 1.99 (0.10)
f/30 NO3- 3.43 (0.31) 40.83 (3.95) 1.20 (0.10)
*, mean of three replicates.
Fig.1. Time course of Alexandrium tamarense cyst production
in batch culture (Three bars indicate three replicates).
Table 2 Time course of f/20 NO3- on cell yield (103cells/ mL),
cyst yield (cysts/mL) and encystment percentage of Alexandrium
tamarense
Cell yield* Cyst yield* Encystment
(SE) (SE) percentage (SE)
1 d 2.15 (0.08) 1.4 (0.15) 0.07 (0.01)
2 d 2.24 (0.11) 1.6 (0.15) 0.07 (0.01)
3 d 2.43 (0.36) 17.7 (3.0) 0.75 (0.20)
6 d 2.51 (0.27) 18.0 (5.9) 0.71 (0.18)
9 d 2.19 (0.23) 24.2 (3.5) 1.12 (0.23)
Control 2.25 (0.12) 17.4 (2.2) 0.78 (0.09)
*, mean of three replicates.
GU Hai-Feng et al.: Cyst Formation, Development of Alexandrium tamarense from Yangtse River Estuary and Its Relation to
Bloom Dynamics 1027
2.2 Cyst maturation
Newly formed cysts were deeply pigmented and com-
pletely filled with starch (Fig.6). They had three thick walls
once formed and began to excrete mucilaginous substance
within 1 d, which formed a ring after several days (Fig.9).
When such a cyst was micropipetted to a 96 well plate for
germination experiments, we observed a new ring form in
several days, meaning that the cyst kept excreting muci-
laginous material. The cyst developed quickly at 20 ℃,
with starch granules decreasing and pigment accumulating
into center in 3 d (Fig.7). Ten days later the accumulation
body was obvious and the dispensed pigment essentially
was gone (Fig.8). Most accumulation bodies were red but a
few were yellow. After 10 d storage at 20 ℃, the cysts
began to excyst. Fifteen days were needed if the cyst was
stored at 15 ℃. The dormancy period of cysts produced
by strains from Guangxi was also ca. 10 d at storage of 20
℃. A planomeiocyte came out of the cyst like an ameba,
with the accumulation body still visible (Fig.10). There was
no definitive conclusion about the shape and location of
the archeopyle of this species. We observed a small round
hole near the pole of the cyst but the hole was difficult to
find sometimes. The cysts can germinate at 20 ℃ without
temperature change, with germination rate of 75.6% 20 d
after formation.
2.3 Cyst dynamics
The A. tamarense cyst density in surface sediment of
DG-26 station dropped to 4.5 cysts/g in August from 31.7
cysts/g in May and rose to 25.8 cysts/g in November of
2002. Cyst density dropped to 0.9 cysts/g in February of
2003 possibly because of germination and rose again to
1.5 cysts/g in May (Fig.2). Nearly all the cysts collected in
November and February were well developed with little
starch and obvious accumulation bodies (Figs.5,13). In
contrast, most cysts collected in May were filled completely
with starch (Fig.11), with a few cysts developing accumulation
bodies (Fig.12). What is more, the total viable cyst density
in surface sediment was much greater than that in other
layers. This proved that dinoflagellates were forming new
cysts, including A. tamarense. But A. tamarense cysts dis-
tributed nearly evenly vertically (Fig.3).
3 Discussion
3.1 Encystment
Anderson et al. (1984) reported that the encystment
percentage of A. tamarense from east coast of the United
States was about 20%, but some strains had low encyst-
ment ability (Anderson personal communication). In our
experiments the maximum encystment percentage was only
2.0. It was possible that the strains we obtained were not
efficient cyst producers or the media used had negative
effect on encystment.
Ishikawa and Taniguchi (1996) reported that sexual re-
production and encystment of Scrippsiella spp. in natural
populations were enhanced by serial, short-term depletion
of nutrients. The mean NO3- concentration in the Yangtse
River estuary was about 20 mmol/L (Liu personal
communication). When the bloom broke out, the number of
cells were able to exhaust nutrients including N in a limited
area, which can induce A. tamarense cyst formation.
About half of the A. tamarense cells encysted in Cape
Cod salt ponds as the bloom maxima approached
(Anderson, 1983). The encystment rate in the Yangtse River
estuary was difficult to estimate since no count of
Fig.2. Alexandrium tamarense cyst density in surface sediment
of DG-26 station from 2002 to 2003 (Three bars indicate three
replicates; Data in May, 2002 is according to Wang and Qi (2003)).
Table 3 Alexandrium tamarense cyst concentration (cysts/
cm3) at different sediment layers of DG-26 station at the estu-
ary of Yangtse River collected in November, 2002 and in February,
2003
Layers (cm)
Time
0-2 2-4 4-6 6-8 8-1010-20
2002.11 23.5 11.4 8.4 13.0 21.1 3.5
2003.02 1.0 3.6 2.3 1.4 14.4 1.2
Fig.3. Vertical distribution of Alexandrium tamarense and total
viable cysts density at DG-26 station in May, 2003
Acta Botanica Sinica 植物学报 Vol.46 No.9 20041028
planozygotes was made during the bloom. We assume that
the cell density was 5× 104 cells/mL and distributed
evenly in water column one meter deep under the surface.
Considering the average cyst density was 15.5 cysts/cm3
and distributed mainly in sediment from surface to 10 cm
depth (Table 3), the encystment percentage was only 0.003.
The data was possibly underestimated because we did not
know how many cysts had been lost through grazing, dif-
fusion and resuspension. To estimate the encystment rate
in the field accurately, two methods might be applicable.
One is to collect water samples and calculate the percent-
age of planozygote, the other is to collect cysts using a
sediment trap and calculate motile cells in the water column.
The difficulty lies in the fact that it is hard to distinguish A.
tamarense from other Alexandrium spp.
3.2 Cyst maturation
A. tamarense can form temporary cysts, which is a reac-
tion to short term harsh conditions such as low temperature,
pollution, and even turbulence (Anderson and Wall, 1978).
Temporary cysts can revive in 1 or 2 d. Resting cysts are
believed to be a mechanism to survive long term unsuitable
environments. In frigid area, cysts of A. tamarense formed
in the fall needed four months or more for maturation, which
helped them survive the winter whose temperature was
lower than 5 ℃ (Anderson, 1980). In temperate and sub-
tropical area, the water temperature in winter is not so hard
for the cell’s survival. The lowest and highest water tem-
perature in Yangtse River estuary was about 10 and 29 ℃,
respectively (Jin, 1992). The water temperature of nearby
Weizhou Island is even higher. The dormancy period of A.
tamarense cysts at 20 ℃ reduced from 30 d in frigid area
(Anderson, 1980) to 10 d in temperate and subtropical zone.
The species does not need to overwinter in these areas,
but the benthic cyst population provides an insurance
against catastrophic events in the plankton (Ishikawa and
Taniguchi, 1996).
In culture plates we found a few round cysts in the
bottom, as also discovered by Anderson (1980). The round
cysts were possibly results of unnatural environment. We
incubated a round cyst from the sediment and found that
the culture produced ellipsoidal cysts in laboratory. Bolch
and Hallegraeff (1990) also found such a round cyst pro-
duced A. tamarense motile cells (as A. excavatum). The
ratio of round and elliptical cysts in the field was not known,
which complicated our understanding of encystment in the
field.
The general pattern of new cyst development was simi-
lar to that reported by Anderson (1980).The procedure
Figs.4-13. 4. A planozygote(50 mm× 43 mm). 5. A cyst from the field collected in November, 2002 (45 mm× 27 mm). 6-8. Cysts
formed in the lab 1, 3, 10 d old (35 mm×30 mm, 35 mm×27 mm, 38 mm×30 mm). 9. A cyst formed in the lab with a ring (45 mm×
37 mm). 10. A planomeizygote (57 mm×51 mm). 11-12. Cysts from the field collected in May of 2003 (50 mm×30 mm, 45 mm×25
mm). 13. Cysts clump from the field collected in February, 2003 (48 mm×35 mm).
GU Hai-Feng et al.: Cyst Formation, Development of Alexandrium tamarense from Yangtse River Estuary and Its Relation to
Bloom Dynamics 1029
involves a gradient loss of pigmentation, leading to the
formation of an accumulation body. Starch grains that ini-
tially fill the cell eventually recede from the poles and leave
a band at the center of the cell. Small particles in Brownian
motion are visible at the poles.
The mucilaginous substance excreted by the cysts might
help their dispersal and survival. Cysts easily adhere to
other particles during sedimentation, which help them to
inhabit wider area. In the cyst map survey in Yangtse River
estuary, we found the existence of Alexandrium cysts in
sandy sediments, where no other cysts were found (Gu et
al., 2003). The mucilaginous layers also help cysts clump
together, which possibly made them difficult to be ingested
by benthos animals. We discovered such a clump of four
cysts in the sediment sample (Fig.13). Such clumps might
be abundant in the field as sonication could separate them.
3.3 Cyst dynamics
The seasonal variation of cyst abundance reflected the
encystment and excystment of A. tamarense in the Yangtse
River estuary. In May of 2002, there was large scale bloom
of Prorocentram dentatum accompanied by high density
of Alexandrium spp. (Wang and Huang, 2003). The bloom
resulted in high cyst density in surface sediment, up to
31.7 cysts/g at DG26 station (Wang and Qi, 2003). Most of
those cysts had germinated by August, and a fraction of
cysts might remain in the sediment because of anoxic envi-
ronment (Anderson et al., 1987). Wang and Hong (1994)
reported that there was no A. tamarense cyst in the sedi-
ment of this area, possibly because they collected sedi-
ment in the summer and cysts had germinated at this time.
There was no official report of Alexandrium bloom outbreak
in fall of 2002, but we suspect that it might happen based
on the sudden cyst density increase from August to
November. There was large scale P. dentatum bloom in
May, 2003 without high density of Alexandrium sp. This
can explain the low Alexandrium cyst density in surface
sediment in May, 2003 compared to that in 2002.
3.4 Inoculum size
A very small proportion of germinating cysts is suffi-
cient to initiate a bloom if the timing of germination coin-
cides with favorable growth conditions (Ishikawa and
Taniguchi, 1996; Anderson, 1998), while some species in-
vest great numbers of cysts to establish a small inoculum
population under unfavorable conditions (Kremp, 2000).
A. tamarense in the Yangtse River estuary seemed to fol-
low both of the two strategies. The average cyst density in
November, 2002 was 15.5 cysts/cm3, and dropped to 4.5
cysts/cm3 in February (Table 3) and nearly zero in May,
2003. Considering the high germination rate, about 90%
(Gu et al., 2003) and the water depth is ca. 50 m at this
station, the germination of cysts from November, 2002 to
February, 2003 provided the inoculum size of 98 cells/L.
From February to May the size was about 44 cells/L.
Alexandrium spp. cells were not discovered in the wa-
ter column during the survey in February, 2003, but they
appeared in November and May, although the number was
low. The germination of A. tamarense cysts might contrib-
ute to the winter population greatly, but the water tempera-
ture was too low for the cell’s growth. The inoculum size of
A. tamarense cells in the early spring of 2002 is not known.
The number should not exceed that of 2003 since a large
bloom broke out in fall of 2002 and left many cysts in the
sediment. The largest bloom, however, was in 2002, not in
2003. Our study supports the view that the inoculum size is
not a major factor to determine the outbreak of bloom
(Blanco, 1995; Rengefors, 1998).
Acknowledgements: We gratefully acknowledge Dr. GAO
Ya-Hui in Xiamen University for providing sediment and
water samples. Dr. D. M. Anderson in Woods Hole Ocean-
ography Institute was thanked for carefully reviewing the
manuscript and giving out constructive suggestions.
References:
Anderson D M, Wall D. 1978. Potential importance of benthic
cysts of Gonyaulax tamarensis and G. excavata in initiating
toxic dinoflagellate blooms. J Phycol, 14: 224-234.
Anderson D M, Morel F M. 1979. The seeding of two red tide
blooms by the germination of benthic Gonyaulax tamarensis
hypnocyst. Estuarine Coastal Mar Sci, 8: 279-293.
Anderson D M. 1980. Effect of temperature conditioning on de-
velopment and germination of Gonyaulax tamarensis
(Dinophyceae) hypnozygotes. J Phycol, 16: 166-172.
Anderson D M, Chisholm S W. 1983. The importance of life
cycle events in the population dynamics of Gonyaulax
tamarensis. Mar Biol, 76: 179-190.
Anderson D M, Kulis D M, Binder B J. 1984. Sexuality and cyst
formation in the dinoflagellate Gonyaulax tamarensis: cyst
yield in batch cultures. J Phycol, 20: 418-425.
Anderson D M, Taylor C D, Armbrust E V. 1987. The effects of
darkness and anaerobiosis on dinoflagellate cyst germination.
Limnol Oceanogr, 32: 340-351.
Anderson D M. 1998. Physiology and bloom dynamics of toxic
Alexandrium species, with emphasis on life cycle transitions.
Anderson D M, Cembella A D, Hallegraeff G M. The
Acta Botanica Sinica 植物学报 Vol.46 No.9 20041030
(Managing editor: HAN Ya-Qin)
Physiological Ecology of Harmful Algal Blooms. Heidelberg:
Springer-Verlag. 29-48.
Blanco J. 1995. A model of the effect of cyst germination on the
development of the Gymnodinium catenatum population on
the west coast of the Iberian peninsula. Lassus P, Arzul G,
Erard E, Gentien P, Marcaillou C. Harmful Marine Algal
Blooms. Lavoisier: Technique et Documentation. 563-566.
Bolch C J, Hallegraeff G M. 1990. Dinoflagellate cysts in recent
marine sediments from Tasmania, Australia. Bot Mar, 33:
173-192.
Doucette G J, Harrison P J. 1989. Cyst formation in the red tide
dinoflagellate Alexandrium tamarense (Dinophyceae): effects
of iron stress. J Phycol, 25: 721-731.
Godhe A, Norén F, Kuylenstierna M, Ekberg C, Karlson B. 2001.
Relationship between planktonic dinoflagellate abundance,
cysts recovered in sediment traps and environmental factors
in the Gullmar Fjord, Sweden. J Plankton Res, 23: 923-938.
Gu H-F, Lan D-Z , Fang Q , Wang Z-L , Cai F. 2003. Distribution
and germination of Alexandrium spp. cyst in Southern East
China Sea. Chin J Appl Ecol , 14: 1081-1084. (in Chinese
with English abstract)
Hallegraeff G M. 1993. Review of harmful algal blooms and their
apparent global increase. Phycologia, 32(2): 79-99.
Ishikawa A, Taniguchi A. 1996. Contribution of benthic cysts to
the population dynamics of Scrippsiella spp. (Dinophyceae)
in Onagawa Bay, Northeast Japan. Mar Ecol Prog Ser, 140:
169-178.
Jin X-L. 1992. Marine geology of East China Sea. Beijing: Chi-
nese Ocean Press. 16. (in Chinese)
Kremp A. 2000. Distribution, dynamics and in situ seeding po-
tential of Scrippsiella hangoei (Dinophyceae) cyst popula-
tions from the Baltic Sea. J Plankton Res, 22: 2155-2169.
Li R-X , Xia B. 1995. Two toxic dinoflagellates in Jiaozhou Bay:
Alexandrium tamarense and A. catenella. Zhu M-Y . Proceed-
ings of the Second Meeting of Chinese Committee of SCOR-
IOC HAB Working Group. Qingdao: Qingdao Press. 36-41.
(in Chinese with English abstract)
Morey G G, Ruse R H. 1980. Encystment and reproduction of
the predatory dinoflagellate Polykrikos kofoidii Chatton
(Gymnodiniales). Phycologia, 19: 230-236.
Olli K, Anderson D M. 2002. High encystment success of the
dinoflagellate Scrippsiella cf. lachrymosa in culture
experiments. J Phycol, 38: 145-156.
Rengefors K. 1998. Seasonal succession of dinoflagellate coupled
to the benthic cyst dynamics in Lake Erken. Arch Hydrobiol
Spec Iss Adv Limnol, 51: 123-141.
Wall D, Guillard R R L, Dale B. 1970. Calcitic resting cysts in
Peridinium trochoideum (Stein) Lemmermann, an autotrophic
marine dinoflagellate. Phycologia, 9: 151-156.
Wang W-P, Hong J-C. 1994. Preliminary study on distribution of
dinoflagellate cysts in neritic surface sediments of East China
Sea in summer, 1992. Mar Sci Bull , 13(6): 53-59. (in Chinese
with English abstract)
Wang J-H , Huang X-Q . 2003. Ecological characteristics of
Prorocentrum dentatem and the cause of harmful algal bloom
formation in China Sea. Chin J Appl Ecol, 14: 1065-1069. (in
Chinese with English abstract)
Wang Z-H, Qi Y-Z . 2003. Distribution of dinoflagellate resting
cysts in surface sediments from the Yangtse River Estuary.
Chin J Appl Ecol, 14: 1039-1043. (in Chinese with English
abstract)
White A W, Hewis C M. 1982. Resting cysts of the toxic, red tide
dinoflagellate Gonaulax excavata in Bay of Fundy Sediment.
Can J Fish Aqua Sci, 39: 1185-1194.
Zingmark R G. 1970. Sexual reproduction in the dinoflagellate
Noctiluca miliaris Suriray. J Phycol, 6: 122-126.