JARQ 33, 283- 293 ( 1999)
Harmful Effect of Dinoflagellate Heterocapsa
circularisquama on Shellfish Aquaculture in Japan
Yukihiko MATSUYAMA
Harmful Algal Bloom Division, National Research Institute of Fisheries and Environment of
Inland Sea (Maruishi, Ohno, Saeki, Hiroshima, 739-0452 Japan)
Abstract
The marine dinoflagellate Heterocapsa circularisquama Horiguchi is the causal agent of red
tide on the Japanese coast. In the last decade, H. circularisquama red tides have destroyed
the shellfish aquaculture industries around the western part of Japan because this dinoflagellate shows a detrimental effect on shellfishes particularly on bivalve molluscs. The current
proliferation of H. circularisquama throughout western Japan is a cause for concern due to
economic loss. The outbreaks of H. circularisquama are closely related to the environmental
conditions: water exchange rate, water temperature, local and global climate changes.
Administrative measures such as algal monitoring systems can be successfully utilized for
the distribution and short-term prediction of red tide due to H. circularisquama in several
locations. However, secondary damage, i.e. decline of demand due to misinformation and
cost of measures to prevent the damage, adversely affects the development of shellfish
aquaculture even if direct killing of the products can be avoided.
Discipline: Animal pest / Aquaculture / Fisheries
Additional key words: red tide, bivalve, toxicity, secondary damage
Introduction
Worldwid e development of harmful algal blooms
causes serious problems for public health and fisheries inclustriesL·15•21•23 ·24 >. On t he Japanese coast,
new marin e din oflagc ll alc Heterocapsa circ11/arisq11a111a H origuchi9>, appeared in 1988 and thern
rapidly expanded over th e wes tern area. The red
tide due to /-1. circ11/arisquama has da maged shellfish aquaculture in mos t o f th e rcgion 3 · 12 · 14·3 u 7>.
Although H. circ11/arisq11anw blooms mainly affect
bivalve aquaculture , no harmfu l effects on wild
and cultured fish, other marine vertebrates, and public health haza rd were recorded. Therefore, this
phenomenon is referred to as " novel reel tide".
Incidence o f this species has increased recently,
and the economic losses in aquaculture have been
a ca use for concern for th e industry and society' 4>.
In th e present paper, environmental con ditions
conducive to the red tide occurrence, review of damage caused to aquaculture, toxicity of the organism, and recent monitoring programs based o n
scientific data arc outlined.
E nvironmental conditions causing Heterocapsa
circuI arisquam a bloom
I) Coastal ct1rrents and water exchange rate
Fig. l shows the distribution of red tide events
due l o 1-/. circ11/arisq11a111a (> 106 cells L- 1) on the
Japanese coast. If. circt1!arisqua111a is distributed
over the wes tern part of Japan, especially on the
southern coast of Mie, western coast of Se to
Inland Sea, and western coast of Kyushu I sland.
T he most freque nt area for red tide is Ago Bay,
where H. circularisquama has been observ ed
every year since 1992. The areas where /-/. circularisquama blooms were recorded are embayments
affected by the warm curre nts: Ku roshio and
Tsushima currents (Fig. I).
The red tid e caused by /-/. circularisquama is
commonly observed in semi-closed bays, such as
Ago Bay, Ura nouchi Bay, and Hiroshima Bay.
Dense assem blages of H. circularisquarna cells
have been found in th e innermost part of the
in lets. but not offshore and in the channels. T he
distributi on pattern of /-/. circularisquama seems
284
.JARQ 33(4) 1999
f
t
Omura;;~95)
t
t
0
•
No damage to fisheries
Damage to fisheries
Fig. l. lt c(:Ords of red tid e (>'ID<, cells L-') due to lleterocapsa circultll'isquama in western .Japan
(1)
4
1 Q6
E
~
.!!l
::,
.g
(.)
(1)
V)
e~~
l
f
_
:.,
Q)
Ol
C
11$
...
0-
·~
--.s
10s
....
(ii
3
.!!! 104
Q)
:
.3,
:. .
-0
:;::,
E
E
:::,
·~
1Q3
..
..
..
2
..·.:..
:
•
1 Q2
1Q1
Aug.
~
1
Sep.
Oct.
Nov.
Fig. 2. Relationship between cell densities of /Jeterocapsa circ11farisq11ama
and maximum fidal range in O hno strait, Hiroshima n ay in 1997
Maximum tida l range correspond to the daily he ight ranges be twee n
high ~nd low sea leve l. //. circ11/11risq11a111a popula tion increases
during the nea p tide pe riod a nd decreases durin g the spring tide
perio d.
to be strongl y affected by the water exch ange
rate. N atural populations of /1. circ11/arisr111ama
cel ls significant ly increase dur.ing th e neap tide
and decrease during th e spring tide (Fig. 2). T his
observati on clearly indicates that /1. circ11larisq11a111a popu lati ons arc rel eased f rom semi -cl osed
bays into the offshore zone responsible for spring
lidal current. Simi lar find ings have been report ed
in Alexandri11111 1r111wre11se blooms on the M aine
coast 2l and Gy11111odi11i111n 111ikin101oi in Gokasyo
Bay27l . Therefore. water exchange mainly influences
th e horizonta l dist ri bution and th e pe ri od ic
ch anges of reel t ide due to /-/. cir cularisqua11w and
oth er harmful algal species.
Y. M111suym1111: /111rmf11/ £/feet of Di11ofl11gel/111u Hclc1·ocaps.i circularisqu.111rn 1111 Shellfish i11
J"t>""
285
risq11w1w seems 10 he a species of tropica l or subtropical origin.
2) Waler temperature and salinity
Red tid e associa ted with II. circ11/arisq1.1(1111a
occurs between July and November in the embayments or western Japan. In Ago Bay, the water
temperature and salinity level during the H. circ11/arisq11ama bloom ranged from l5 lO 3 1°C and from
24 to 34 psu. respectively"'l. Generally, H. cirwlarisqum11a blooms appear mainly under high water
temperature (>23°C) and salinity (>30 psu) condi tions. The results of field surveys show Lhat 1-/.
circularisqtu111w grows well under high water and
salinity condi t ions.
Based 0 11 laborat ory culture experiments, opt imal growth of H. circ11/arisq1101110 occurred in a,
combi nation o f wa ter temperature of 30°C and
sa linity of 30 psu. However, the growth o f' fl.
circ11/ari.HfL1a111a decreased significa nt ly below
15°C31 >. These growth responses to temperature and
salinity obtained in laboratory culture correspondl
lo those recorded in field su rveys. On the other
hand. the opt ima l growth of representative lrnrn1ful 11lgae (/\ l exo11dri11111 1amare11se, Chartonella
3)
Verticol mixing of seaivater
Field surveys revea led that temporary seawater
mixing and concom itant upwelling of bottom
water enhanced the proliferation of JI. circularisquama blooms. In Ago Bay, strong distUJbanccs
of water strntification by typhoons preceded th e
red tide outbrea ks of /-/. circ11/arisq11a111a in summer (Fig. 3). In the 1988 red tide at Uranouchi
Bay, a large-scale intrusion of oceanic w11 1er into
the bay and res ultant seawater m i xing were
observed before th e occurrence of red tide due 10
l!. circ11farisq1w111a 18l. In the western part of Seto
In land Sea, where water columns are very stable
due 10 stratification, H. circulari.1·q11a111a bloom hardly occurs in early Lo mid-summer. H owever, in
autumn when the stratification begi ns to break
down clue to ihc decrease of Lhe surface water
temperature, /-/. circ11/t1risq11a1110 frequently causes
red tid e i n cmbayments 15 l . Tcmpornry or sust11inecl water mixing throughout the water column
may provide nut rients and growth-promoting substances from the bou om to the euphotic layer,
resulting in increased salinity. Thus, the proliferation of //. circ11larisq1w111a in coas tal areas is
consi dered to be triggered by vertical mixing of
seawater.
antiq1w, Gy11,nodi11i1t111 111iki11101oi, !-Jeterosigma
akashiwo , etc.) which often cause red tide on the
Japan ese coas t occurred in a combination of
water tempernlure from 15 to 25°C and salini ty
ranging from 20 to 25 psu, respectivelyn-l3•35.3t•>.
On the coas t of western Jap,111, since the maximum water temperature seldom exceeds 30°C, the
growth pattern of 1-l. circ11ft1risqua11w in relation to
the water temperature is different from that of other
harmful algae appearing o n the Japanese coast.
Based on these physiological characters, 11. circula-
4) Co111petirio11 with other phyropla111<1011 species
The compe titi on between //. circ11farisq11t111111
and oth er microalgae is also noteworthy. According
to fi eld observaLions carried o ut ove r a 3-year
101
101
1992
32
e_ 30
10•
106
~
;a 28
•...J
10S .!!l
iii
0
104
'...I
~
Q)
105 ~
E26
Q)
0
2
2
"'
~
24
104
22
<103
<103
Heterocapsa circularisquama
--Om ··· .. ·2 m - ··-Sm ---7m
W)u44}J
Heterocapsa circularisquama
- -0 m ··· · .. 2 m -··- 5 m --- 7 m
Fig. 3. Change~ in waler lcmpcral u rc al 4 diffe re nt d epths an cl mean ce ll density of N eterQCllJ>Sfl
circularisqutmw in Ago Hay
Arrows tlcnote the typhoon events (Matsuyanw cl c1l.. 1996).
286
JARQ 33(4) 1999
period in Ago 13ay, the growth of H . circu/arisqunmn occurs when the populmions of dominant
diatoms Clwetoceros spp. begin lo decrease (Fig.
4). Maxim um yield and duration of H. circ11/arisq11a11w bloom seem 10 be strongly affected by
the Chnetoceros spp. populations. Il is considered
that the decrease of t he dominant diatom populat ion is conducive 10 /-/. circuforisquanw growt h.
Uchida et ai.2'1> reported that th e growth of fl. cic11/arisq11.t1111a was suppressed under bialgal cu ltures
with diatom species including Chaetoceros didy11111111,
Stepluwopyxis pa/merinna and Licm opho re sp.
Under the effect of diatoms, th e cells of 1-1. circula-
5)
107
106
'~ 10
1993
~
.A
6,
_J
...
A
'6.
5
(I)
0
6
'C:
't-:
..
10'
b
10•
July
June
Sep.
Aug.
107
6.
!..J
106
•'I'.,
"t,·
'ti.
, b . t,,
.
1994
fl. '(J. ""·.
IS
~ 105
(I)
0
104
103
July
June
107
.
6.
6
10
!..J
ri.u1u11111a became rnund to c llip1ical and were
considered 10 be temporary cysts. I l is assumed
that diatom populations regulate the development
and decline of red tide due to / /. circularisq11a11w.
Fu rther more, 1-1. cirrnlarisq11a111a was found to
kill a mixotrophic dinoflagellate Gyrodi11i11111 i11s1riat11111 and tintinnid ciliate Favelln taraikaensis 102N>.
The results show th at H. c:irc11/arisq11m1w is toxic
10 active predators and competitors. From the
ecological point of view, this characteristi c might
be advanrngeous for bloom formation in na i urnl
envi ronm en1s111•1~J,
Sep.
Aug .
1995
'A,
/!.
6.
f>' •A
~ 105
(I)
A
0
10'
..A •..:S
A
.
•'
ti
103
June
July
Aug.
Sep.
Fig. 4. Changes in cell densities of lleterocapsa circ11/arisq11t1111a (P) 1111d predominant diatom Clwe((Jceros
sp1>- (g) iJ1 Tatcgami hdet, Ago Bay (1993-1995)
/-I. circ11/arisq111111111 fre<1ue111ly appe.1rs when
1he popu lation of Cl1ae1ocero.1· spp. is low
( niche) which is probably due to the high water
temperature and strong strntification. Massive
bloC>m (>IO'' cells L 1) and concomitant death
C>f pc11rl oyster were observed du r ing th e
1994 bloom period. The data sets were provided in part by T. Kobayashi. Mic Prefcctural
Fisheries Tcclrn ical Center.
Long-term trend of Heterocapsa circularisquanrn
blooms
The records of red tide due to II. circ11/arisq1111111a
arc shown in Fig. 5. T he red tide incidence associated with / /. circ11/arisquanw has rapidly increased
since the early 1990s. Why can JI. circu/arisq11a111a
appear and colonize the Japanese coast? Laboratory experim ents reveal that /-/. circ11/arisq11ama
can 1101 grow at 10°C or less.11l, and does not form
typical rest ing cysts that can survive below 10°C
(Uchidc1 & Ma tsuyama, unpub. data). Hence, the
overwintering vegetative cells are the likely seed
populat ion fo r bloom initiation of thi s species.
This growth strat egy is considered to be disadvantage<lus for the occurrence of this species in temperate and cold seas.
On the Japanese coast. howeve r , the water
temperature in winter has significantly increased
since th e late J980s 11 ), probably d ue to global clinrnle change (green house effect and E l Nino phenomenon). Recently, the tropic;i l ;ind subtropica l
dinoflagellate Proroce111r11111 sigmoides Boh m has
freq uently appeared in western Japatr101• I n the Seto
Inland Sea. th e water temperature in winter considerably increased in the last decacle, except for
the peri<>cl 1995- 1996 (Fig. 5). Acc<lrdingly, tropical marine animllls. e.g. green shell mussel Pema
viridis, have f requenlly appea red in t he Seto
Inl and Se,1 since th e early 1990s. T his hydrographic change may be conducive 10 the overwi nteri ng of II. circ11/arisq11r1111a on t he Japanese
coast. The rela tionship between the wa ter temperature in wint er and initial occurrence of red
tide clue to th e di norlage llate C. mikimotoi was
also observed in the previous study'>. Hyclrographic
change in lerms of w,ller lemperalllre is likely to
bring about changes of the ph ytoplankton com munities in th e Japanese coastal wat ers.
Y. Mt11s11y,111w: N111'111f11f Effect of Di11oflngellfll~ Mctcrocapsa circularisq11i11na r111 Sl1el/Ji:,1, in
287
lt1flllll
~
Cl:!
E 8
0 Cl:!
-:::,
Cl)
0-
::J -~
ro
::J
.....
11 .0
7
Cl)
6
10
·-"'O (.)~
5
9
Cl:!
4
"'O
i....:
-S!
"'O:::,
Cl)
-·(l)
..... Cl)
-Q
ro
~
Cl:!
ce
!
(.)
<(~
~
- - - - - - - - - - - - Mild winter
.,
·.:,
.,...
8
-0
3
2
-0
...
7
0
-0
0
...
0
C
0
~
co
oco
.... Ol
~
....
.!:
(l)
.....
::J
ro.....
(l)
a.
E
(l)
.....
Cl)
6
"~
1
LL
(X)
(X)
C1)
,-
C1)
co
C1)
,-
0
C1)
C1)
,C1)
C1)
C\I
C1)
C1)
C')
C1)
C1)
<t
C1)
C1)
..-
ll)
C1)
C1)
..-
<D
r-C1)
,-
,-
C1)
C1)
C1)
<X>
C1)
C1)
5
+-'
ro
~
i
,-
Fig. 5. Long-term tre nd of red tide eve nts du e to Jfeterocapsa circ11/arisquama in .Japa n and winter
water le mpe (atnre ( February) in e aste rn Seto Inland Sea ( Hurimu-nada)
T he data sets or wate,· tempera ture were provided by Y . H o ri. Hyogo Prcfccturnl
Fishe ries Experimental Station.
6)
Possible origin
There have been no records of H. circ11/arisq11a111a
reel licle and related shellfish mortality in Japan
before 1988. It remains to be determ ined whet her
!-I. circu/arisquama is a native species of Japan.
Considering the growth response to water temperature, it is possible l hat JI. circularisqur1111a originaIes from tropical or subtropical regions, and
has recently invaded Japanese coastal areas by
warm current and /or artificial transpo rtati on.
Recently, simulated experiments have reveH led lh,ll
fl. circularisquama could easily migrate to distant
Meas in association with shellfish tran sportation8>.
During the last 2 decades. large shellfish spats, especially pea rl oyster and short-necked clam, have been
imported to Japan from Southeast Asia for aq uaculture. It is therefore possible that 11. circ11/arisq11t1ma invaded Japan from tropical or subtropical
seas (T. Honjo, pers. commu n.). However, further studi es should be ca rried out to analyze the
artificial dispersal of H. circu/arisq11m11a.
Damage to fisheries and toxicity
I ) S/u:1/j,sh damage to aq1.1ac11/11.1re industries
Jn September 1.988. extensive red tide clue to
H. circu/arisqnama and subsequent death of short-
necked clams Ruditapes philippinarum occurred in
Uranouchi Bay, Kochi Prefecture (Table I). Reel
tide due lo/-/. circ11larisq11a11·1r1 occurred at Fu kuoka
Bay i n 1989, and al A go Bay in 1992, resulting in
high mortality of shellfish13·.1·1>.
Until l 998, 26 cases of H. circ11/arisq11mna red
tide ( including 15 incidences leading to fisheri es
damage) had been record ed in 14 locat io ns of
western Japan (Fig. 1). The red tide due l o /-/.
circ11/arisq11a111a was associa t ed with massive
killing of commercially imporian! bivalve species:
short-necked clam R. philippinamm , pacific oyster
Cra.1·sos1rea gigas, pea r l oyster Pincwda fucaw ,
blue mussel /YIy1i/11s galloprovi11cialis, etc. 1\ 14·'01>.
The current proliferation of fl. circularisq11a111a
throughout western Japan destroyed the local shellfish mariculture. Economic losses of shell fish aquaculture by direct killing of marketable products were
estimated to amount to about at least IO bi llionyen in the last decade.
On lhe other hand, there are no records of dea th
of finfish and cru stacean species or public health
hazard clue lo the consumption of shel lfi sh Hncl
other sea rood products in association with the
red tide of H. circ11/arisq11ama 11•>. This type of biohazard in marine animals is markedly differen t
from previous damage caused by harmfu l algae
responsible for parnlytic shellfish poisoning ( PSP),
288
JA RQ
33(4) 1999
T 11hlc 1. Records of d11magc to s hellfish s pecies d ue to red tide associated
wit h N eterocaf)l'(I circ11larisq11t1111a in western J a pan
Da te
Shellfish species affected
1988
R11diwpes phi/ippinamm
1,560 t losses
Uranouchi Bay
1989
Cmssostrea gigas
Mm:rm clti11l'11si.r
My1i/11s galloprovinciolis
f< tu/ilttf)l'S phlfippillll/'11/11
So/e11 s1riclll.f
mass mor tality
Fukuoka Bay
34
1992
Pi11 cwda f 11c11111
30- 90% mor1a li1 y
loss or > 18 million indi vidmils
Ago Bay
13
Cmssosrrca gigns
lv/ytil11s galloprovi11ciali.1·
Cltlt1111y.f 11ohili.r
mass mortalit y
R11di1apes pltilippi11111w11
Cmssosll'l:a gig11s
50- 90% decrease of harvest
1994
Pi11clllda f uc:11111
40- 90% 111ortali1y in areas wi1h
ex tensive assemblages
Ago Bay
14
1994
Pi/1(:wda f 11c:a111
mean 65.4% 111or1ali1y in
2 yea r~ olcl individuals
mean 69.5% mortality
mass mortality
K usu-ura Bay
37
Pi11cu1da f 11,·t1111
5- 36% monality
Ago Bay
Cm.1·sos1rea gigns
R11di1apes pltilippi11ar11111
My1i/11s gallopmvi11cialis
36- 68% mortalit y, 6 10 r losses
>70% mortality, 2 10 t losses
I0- 55% mortality
Hiroshima Bay
1996
Pillcwda fuca //1
111ass mon ality
losses or 1.5 milion individuals
Ago Bay
1997
Pi11crrul11 f11c11111
Cmssostrea gigas
My1il11s gt1/loproi•i11ci11/is
mass 111onality
Obama Bay
Crassostrl'tt gigas
Myti/11s g11/loprovi11dalis
S11/c11/11s diver.ficolvrs
mass 111ortali t y i11 spats and adults
75% 111ort,1lity i n assemblage areas
111ort ality in matural populat ion
Hiroshima Bay
Rud itt1pes pltilippi11am111
2 lO t losses
13u.cen Sea
Rudiu,pes phi lippilwn1111
Cmssosrrea gigas
lV/111: tra ve11erifon11is
50'¥" decrease or spa1 yield
Suo-n ada
Crnssostrea gigas
Hiroshima 13ay
Ruditapes pltilippi1111n1111
30- 98% mortalit y
ca. 5,000 1 losses
50- 90% mortalit y
1\ 1ri1111 pccti11a/1t
considcrnblc mon ality
Suo-nacla
1993
l?udiu,pes pltilippi1111n1111
Cra.rsosll'l'II gigas
Solen .wric111.f
MIIC/1'11 VCIIIJl'ijOr//l iS
M11sculista .rn11!tousitt
A11011wlorn rdi/1 /If/ 11r1111M11.t
D 0si11or//is japo11ica
Glnss1111/11x didy11111
1995
1998
Notes
Location
Reference
Lak e Hamana
mass monality
considerable morrnlity
The data se ts we re obuiined from Fishery Regulat ion Office, Fisl1cri es Agency of Japan.
15
3
)'. Ma1rnym11a: l/11r111f11/ Effec:t of Oi11oflagel/111e Hc1crocapsa circularist1m1 11rn 011 Shellfish in J11p1111
diarrheic shellfish poisoning (DSP), amnesic
shell fish poisoning (ASP), neurotoxic shel l rish
poison ing (NSP), eiguatera poisoning, and ichthyoloxicity.
2)
General c/1arac1eris1ics of shellfish affected by
red fide
T he effects of H. circularisquama on bivalve
molluscs were described in previous studies~-1~· 15•1'i).
Malsuymna c t al. 1"> observed that exposure of
pearl oysters to 5- 10 X 106 1-/. circ11/arisq11.ama
cel ls L· 1 resulted in death within severa l clays
although the level of dissolved oxygen was not
critica l. The dead individuals were characterized
by a marked shrinkage of the mantle, decrease of
glycogen lobe attached to the mantle and gut discoloration (Fig. 6). The symptoms clearly reflected the direct cyto toxic effect of H. circularisquanw
on pearl oyster physio logy. Similar harmful
effects on oyster C. gigas and the mussel M. galloprovincialis were observed during the red Lide
which occurred in Hiroshima Bay15'. Based on
detai led field suJveys, in most of the bivalve species,
289
the filtration rate is significa ntly reduced at a
density of 5- 20 X Io·• H. circularisquama cells L· 1•
As a result, alterations of bivalve physio logy
clearly sta rted from a cell density below 1%.
3)
Exposure experiment using cul/ured strain
Nagai et al. 19> showed that the mortality of
pearl oyster spats by H. circ11/arisq11ama depends
on the cell density of this alga. Pearl oysters
exposed lo H. circularisq11ama cells at a density
above 107 cells L I showed an unusual contraction
of the mantle and gills, clapping, sustained valve
closure. paralysis. and heartbeat stop with in 24 h.
Furthermore, the mussel M . galloprovincialis sign irican tl y reduced its feeding activity when exposed
to IO" cells L- 1 of H. circu/arisqur,ma, but not in
cu lture with 106 cells L· 1 of morphologically similar dinoflage llates Scrippsiel/a trocl,oidea and
Heterocapsa 1rique1ra 16>. Some harmful algae are
known to be toxic to marine shellfish. The blooms
associat ed witb the unarmored d ino fla gella l e
Gyrodinium cwreolwn and picoplankton A ureococcu.1·
(1110phagefferens referred to as "brown tide" lead
A
Fig. 6. Photographs of pc11rl oyster Pinctada fucata 11ffcctc d by Hetc rocapsa circuh1risq ua11111 in 1992
A: Dead pearl oysters. B: Individual cultured at site wi thout red I ide.
C: Individual cu ltured Hl site with red tide.
290
JARQ 3:\(4) 1999
lo co nsiderable failure in mussel and scal lop
rarmingm. Laboratory- rearing experiments using
th ese algae showed considerable detrimental
effects on various bivalve species 12•20·?~1. However.
th e effect of these harmful algae on marine animals
is not species-specific. Reel tide due lo C. n11reo/um
kills not on ly sh ellfi sh but also l'infish and
crustacea 11 spccics 2''i. A II hough N. circ11/ari.w111w1w
frequ ently kills various bivalve species within a short
period of tim e ( <24 h) as described previously" ·1'1!,
no dca1h and adverse errccls were observed in finfish
and crustacea ns. These facts suggested t lrnt lhe
harmfu l effect of Tl. cirrnlari.1·q11a11111 on bivalves is
specific and pronounced compared lo other harmful
algal species (Table 2).
4)
I larmf11/ ej]ec1.v of Hcterocapsa circularisquama
011 mher animals
Laboratory exposure experiments showed that
various m arine animals such as bivalves. gastropod s171 . solita ry acid ians . and j e l l y fi sh are
alTcctcd by 1-1. circ:u/ari.H/Wlllla un like vertebrates.
crus tace<1ns. starfish, ,111d sea urch ins (Table 2) .
On the other hand, alth ough the occu rrence o r i llness associated with th e consumption or bivalve-s
that accumulated //. circ11/arisq1111111a cel ls may be
a cause ror concern in humans, shclll'ish poisoning
has never b een observed in samples collected
rrom red tide areas. Direct I IPCL ana lysis failed
Lo detect PSP toxin s or DSP tox ins in the cells of
II. circ1.1/arisq111111111 11•>. No dea th or symptoms
were observed in S mice to which a cultured cell
pellet or /I. circularisqum1111 had been injected in
intraperiton eally al a rate o r 10'' cells individuol 1.
5)
C/wmc1erizatio11 of H etcrncapsa ci rcularisquma
1oxici1y
Nagai ct al. 1"1 suggcs1cd th at 1he toxicity of//.
circ11/arisq11a11u1 to bivalves was mediated by a chemical agent. Thereafter, i.l was shown thal Lhe toxic
effect of H. circ11/arisq11m1111 on bivalves was not due
t o extracellular m etabo lites. cell cx ud ates. and
·'naked ce lls" prepared by so nica t ion rnHl centrifugation. Funhcrmorc. trypsin and SDS (sodium
dodecyl sulfate) trea tm ents were found l<> decrca~c
drastically the toxicity of H. circ11/arisq1u111/(/ cells
(Fig. 7). Therefo re, labi le protein-like complex
localized on the cell surfclce pre- sumably exerts a
detrim ental effect on bivalves 11•1• However. purifica tion and characterization of toxic fractions have
1101 been successful because this agenl is highly labile
under neut ral conditions.
6) Secondary da111age to .f7slteries ind11.1·tries
Secondary damage to fisheries nrny occur dllring the //. circ11/arisq11m11a red tide periods. sometimes ca u sing serious econ o mic losses.
As
men l ioncd above. //. cil'Cularisqurmw bloom does
1101 cause human i llness associated with the consumpl.i<)n of harvested products. This fact sho uld
he recogn ize d and fish ermen and consumers
should he informed 11ml " shellfish killing" during
reel t ide du e to II. circ11/arisq11r1111a is different
from ·'shellfish poisoning" due to toxic dino fla gc l lat e b l ooms such as tho se or th e genera
11/e.rn,ulriwn, Gy11111odi11i11m, and Dinophysis. Mis-
T ahlc 2. F. l'fcl·ts of /leteroca11.\'ll circ11larisq11t1111a 0 11 va rio us animals
A nim.ils
cells L- 1
Syrnp1oms
Bivalves
I o·'- 1O'
> 10•
I 0'1- H~'
Feeding inhihilion
Death
Unusual locomotion
Dea th
Fcccling inhibition
Tcniaclc shrinkage
Feeding inhibit ion
Gastropods
Soli tary aciclians
Jell yfish
Protozoa''
Dinoflagcl lc11es
Mouse
Fin fish
Crn h
Lobster. shrimp
Star fish
Copcpods
Di,110 111s
> 10''
> lO''
> I06"
I 0'-106"
>106
> 106
Reference
15, 16
3. 15. 19
17
17
lO
Dea th
I0
D.:ath by cell cont;ict
28
16
> 1()%)
> I 066
> 10'
> 107
> I 01
> 1111
> t ()1
-: Nol .il'fcctcd. ,1) : Specics-$pecific. h): I 111n1pcritoncHI injccl ion.
29
Y. Ma1s11yr11na: //armful Hffcc/ of Vi11oflngcllme I lctcrocapsii circularisqua ma 011 Shcl/jislt i11 J11pt111
29 1
Control
Intact
Trypsin
sos
soc
N=4 mussels
shell height: 25.7± 1.4(S.D.)mm
EOTA
0
50
100
Clearance rate (Control= 100)
Fig. 7. Relative dcarancc rates of M y1i/11s gallo1,rovi11cialis exposed to chcmically treated lle1eroc"ps<1 cir:c ulttrisqtli//1/(/ cells (Control: lsodirysis
galba11a, 8 X 106 cells-')
Initial cel l density or II. c:irc11larisq11r1111a ra 11gcd fr<>m 2.5 - 2.8 X IO'
1
cel ls L· • SDS: sodium dodccylsulfatc. SOC: sodium dcoxycholaie.
[fach chemica l was used al a concc ntrnti<>n lower 1han that wh ich
would inhibit the swimming or /-/. drc11larisq11w1w. E rror bars show
±S.D. $p<0.005 (i· tCst).
info rmati on may lead to a considerable decrease
in the demand for shellfish and market price231 •
Massive N. circ11/nrisq11a111a bloom occurred in a
restricted area of Hiroshima Bay, in 1997. Although
no outbreaks of shellfish poisoning occurred, oyster
demand rapidly declined when th e occu rrence of
red tid e due to /-/. c:ir c11/orisq11anw was broad casted in several TV programs. Market price of
oyster decreased by 10- 30% due lo the decrease
of the demand compared with the previous year.
In t he oyster farm ing industry of Hiroshima Bay.
approximately several hundred persons 11 re employed as oyster shuckers with a low salary. T he decrease of the market price directl y affects shucker
employment.
Monitoring, prediction, ancl methods of
1>revention of red tide
1)
Mo11i1ori11g of red tide due to I-I.
circularisq uama
In Japan, monitorin g systems for harmrul alga l
blooms have been developed by th e Fisheries
Agency and l oca l governmen( orga nizati o ns
( mainl y Prefcct untl Fisher ies Ex pe rim ent al
Stations) since t he early 1970s. These monitori ng
syslems operate successfully and provide inf'orma-
lion on th e inciclc nce of red tid e and shellfish
poison ing as mentioned previousJy21>. Since 1992.
in seveni l locati ons. regular monitoring systems
on Ii. circulariM/IIWlla blooms have been set up.
The local government uses ea rl y warning systems
based on t he data obtained from regular oceanographic surveys. Fishermen arc rou tin ely able to
obtain th e i nformation about harmful 11 lgal bloom
(cell density, water tempernturc, and distribution
of cell assemblages, etc.).
2)
Prevcillio11 of fisheries damage due to I-1.
circularisquama
To our knowledge, it is difficult to con trol or
destroy the large natural populations of reel tide
organisms by applying direct JJrevention methods.
V arious preven ti on techniques (i.e. spraying of
active clay. hydrogen peroxide. and coagulants, etc.)
were developed prcviously6·22l . H owever. widespread applica tion o f these proced ures for marine
env iro nments may exert a secondary harmful
effect on oth er v11luable organisms (i.e. diatoms.
moplankton. fish, benthos, etc.). The simple and
most effeclive method is the tran sfer of cultured
o rganisms from a red tide are<1 lO a non-red tide
area. IJ1 Ago Bay, pearl oyster aquacuhurists began
lo remove the pearl oysters when the cell densi ty
JARO 33(4) 1999
292
of /-/. circult1ri:,y111a111a exceeded about 10~ cells L- 1•
No fis heries damage has occu rred in this bay recently. However, oyster and clam aquaculturists
are still affected by red tide caused by H. circ11/arisquama because the removal procedure is costly
and labor-intensive. As described above, red tide
damage caused by//. circ11/arisq11ama leads to a loss
of marketab le products and secondary damage
such as decrease of demand for the products and
loss of compe ti tiveness in the market due to th e
high cost of the products 10 compensate for t he
cost of prevention of t he damage.
Refe1·ences
1) Anderson, D . M. (1994): Red tide. Sci. /\111., 27].
52- 58.
2) 13alch, W. M . ( 1981 ): An apparent lunar tidal cycle
of phytoplankt on blooming and comn11rn ity succ<:ssion in the Gulf or Maine. ./. Exp. Mar. IJiol. l;'wl..
55, 65- 77.
3) Etou, T .. Kuwamurn, K. & Satou. 1-1 . ( 1998): The
occurrence or a 1/eter ocapsa d rc11fari.vq11r1111t1 retl
tide and subsequent dnmages 10 shellfish in the 13uzc n
Sea in A utumn 1997. /111//. F11k11olw Fish. 1\1/ar.
Tec11ol. Res. Cent.. 8. 9 1- 96 [In Jap1111est:I,
4) H,illcgrae ff, G. M . ( 1993): A review o f harmful
algal blooms and th eir appnrcnl global increase.
Phycologia. 32. 79- 99.
5) Honjo. T. (1 994): The biology and prediction of
rcprescn1a1i ve red tides associated wilh fish kills in
Japan. Rev. Fish. Sci.. 2. 225- 253.
6) H onjo, T. (1994): Overview Oil predic1ion nnd prevention of reel tides ci\usin g dea th o f 1m1ri11c li fe.
r-·ar111i11g Jp11., 28 , 9- 15.
7) H onjo. T . et al. ( 1991): A relationship between
wint er will er tempera ture and the timing or summer Gy11111orlil1i111111111g11.w1kie11s1· reel tides in GokaS}'O
Bay. Nippon S11is1111 Gakkaishi. 57, 1679- 1682.
8) H onj o. T . el al. ( 1998): Po tential l rn nsfe r of
l-leteroc11ps11 cirrnlarisq1111111a with pearl oyster co11si gn111 en1 s. 111 Harmful ,1lgae. eds. Reguern, 8 . cl
al., Xunrn de Galicia & Intergovern mental Ocea nographic Commission of UNESCO, 224-226.
9) Horiguchi, T. ( 1995): 1/eterocap.rn d rwlarisquama
sp. nov. (Peridinialcs. Dinophyceae); a new marine
dinoflagellaie causing mass mor1ali ty of bivalves in
Jnpan. f'ltycol. Res., 43. 129-136.
10) Kami yama, T. & /\rima. S. ( 1997): Letha l effect of
th e di11orlagclla1c /l('(i: ro <·t1psa cirrnlarisq,11111111
upon 1he tintinnicl cil iate Fa,•el/a t11rnik(l(:11.~is. Mar.
£en/. Pmg. Ser., 160. 27- 33.
11 ) Koclanrn . .I .. Nagashima. 1-1. & J;wmi. Y. ( 1995): Longterm variat i ons in th e "Mangoku Herring," Clupea
paflasi Va lcncic1111es resourct:s in rehllion l o ocer111
c11virn11111en1s in th~ waters off S;inriku and Johan.
B11/I. Miy agi Prefect. Fish . Res. Dl'v. Cent .. 14 .
17- 36 l ln Japanese ].
12) Lesser, /vi. P. & Shumway, S. E. (1993): Effects of
toxic dinoflagellates on clearance rates ;111d survival
in juvenile bivalve molluscs. / . Sltellj7sh Res., 12,
377- 38 1.
13) Matsuyama. Y. e1 al. ( 1995):
Eco logical fea tures
and mass mor1,1lity or pearl oysters during the red
tide of 1/eterurnpsa sp. in Ago Bay in 1992. Nippon
Sui.,·1111 Cakkaishi, 61, 35 - 41 [In Japanese with English
summary!.
14) Ma1suya11rn, Y. ct al. (1996): Biological and environm ental aspects of noxiou s clinoflagellatc red
tid es by lfrieroCflf)SII cirwlarisq1111111a in the west
Jiip1111. /11 Hnrmful and tox ic algal blooms. eds.
Yasum o to, T. , Oshima , Y . & Fukuyo. Y ..
Intergovernmental O cea nogrnphic Commission of
UNESCO, P11ris, 247-250.
15) Matsuyama , Y . e1 al. { 1997): O cc urrence of
l-l etl'roc11ps11 circ11farisq11a111a red tid e 11nd subsequent damages to shellfish in western Hiroshima Bay,
Se to Inland Sea, Japan in 1995. !Juli. Nm1sei N(l(I.
n sh. Nes. Inst., 30. 189-207 I'! n Japanese with English
summary I.
16) Matsuyamfl. Y .. Uchida, T . & l-lonjo. T . ()997):
Toxic effects or lhc clinoflagcl l at e N eterocop.rn
circ1tf11risq11a111a on clearance rate of the blue mussel
My1i/11s gaflor>ro11i11cialis. 1\411r. Ecol. Prog. Ser., L46.
73- 80.
17) Matsuyama. Y .. Koi:wmi. Y . & Uchida. T. ( 1998):
E ffect of harmful phytoplank ton on lhe surviv.il of
the abalones, 1/11/iotis disi:us and S11/c11/11s 1/iversicnlor. IJ11/I. Na11.,·ei Natl. Fish. Res. Inst.. 31. 19- 24.
18) Munckage. Y . cl al. (1991 ): Intrusion of external
s11 linc water inrluencing a,wxi c w,ller in Uranouchi
Bay. Nippon S11isr111 Gakkaislti, 57, 1635- 1643 fin
Japanese wi th English summ1Hyl.
19) Nagai, K. et al. ( 1996): Toxicity and LDso l evels of
th e red lidc di11oflagella1c l/eter oc11p.rn circ11fa risqw111111 011 j uvenile pearl oysters. ilq11arnlt11re, 144,
149- 154.
20) Nielsen. M. V. & Stromgren. T . ( 1991) : Shell grow1h
2 1)
22)
23)
24)
25)
2(i)
response of mussels (J\ll ytilus er/11/is ) exposed to
toxic microalgae. Mar. Biol., 108, 263-267.
Okaichi. T. ( 1989): Red tide problems in t lie Seto
Inland Sen, Japan. 111 Red !ides, biol. environ. sci.,
toxicol. eds. Okaichi, T .• Anderson, D. M . & Nemoto.
T., Elsevier. l37- 142.
Shiro1a, A. ( 1989): Reel tide problem and countermeasures. II. /11t. / . llq11a. Fisft. Tech11of.. "I , 195 - 223.
Shumway, S. E. ( 1990): A revi ew or 1he effects of
algal blooms 011 shellfish and aquaculture. ./. World
ilq11ac11/11.1re Soc.. 21, 65- 104.
Smayda, T . ( 1990): Novel and nuisance phytoplankton bloom s in the sea: evidence fo r a globiil
epidemic. /11 Toxic marine phytoplankton. eds.
Grnneli, E. et al .. Elsevier. New York, 29-40.
Smolowi1z. R. & Sumway. S. E. ( 1997): Possible
cytotoxic effects of the cl inoflagellate, Gyrodi11i11111
aureo/11111, 0 11 juvenile bivalve molluscs. Aqw1c11/t11re
Int., 5. 29 1- 300.
Tangen, K. (1977): 131 00111 of Gyrodi11i11111 1111reoft1111
( Dinophyccae) in north E uropean waters, accompa-
Y.
M111s11y1111111:
l/(lr111f11/ Effect of Di11of//1gel/"1~ Hctc,·oc,1psa circularisquunrn
nied by mortality in marine organism. Sarsit,, 62.
123-133.
27) Toda, S. ct al. ( 1994): Effect of w111er exchange 011
th e growth of th e red -tide dinoflagell,11e Cy11111odi11i1111111aga.rnkie11se in an in lei of Ookasyo Bay, Japan.
13111/. Natl. Res. 111st. /lq11acuf111re. Suppl., I , 21-26.
28) Uchida. T. cl al. (1995): The red-tide dinoflagella1e Heterocapsa Sp. kil l~ Gyrodinit1111 i11s1ria111111 by
cell con tact. Mar. Ecol. Prog. Ser., ll8, 301 - 303.
29) Uchida. T . el al. (1996): Growth in1erac1ions between
a red tide dinoflage ll atc Hcueroc11ps11 cir c11la ri.w11111111a and some other phytoplankton species in
cu l ture. In Harmful and t0xic algal blooms. eds.
Yasumoto. T., Oshima. Y . & Fukuyo, Y.,
l ntergovernmental Oceanographic Commission o f
UNESCO, Paris. 369-372.
30) Ueda, 1-1. cl al. ( 1998): Proroce111ru111 sigmoides f36lm
(Dinophyccac) red tide in Unrnouchi Inlet. K ochi,
Japan. 8111/. P/r111ktn11 Snc. .lpn., 45, 149- 153.
3 1) Yamaguchi, M. cl al. (1997): Effects of 1cmpernturc and salinity on the grow th of th e red tide flagella1cs N t:1eroct1p.rn circ11larisq111111111 (Di nophyceae)
and Clrnfl<mella verm c11losa ( Raphidophyccae). J.
P/onk. Res., l9. 1167- 11 74.
32) Yamaguchi. M. & 1-lonjo. T. (1989): Effec ts of
1cmpera1ure. s.tlinity and irnidiancc on the growth
rates of !he noxious red tide flngellates Cy11111odi11i11111
11ng11s11kieuse (Dinophyceae). Nippon S11i.rn11
011
Shellfish i11 Ja1m11
293
Caklwislti, 55. 2029-2036 j In Japanese with English
summary I.
33) Yamaguchi , M ., Im ai, I. & 1-lonjo. T. (1991):
Effects or temperature, salini ty and irradiancc on
the growth rates of the noxious red tide flagellates
Clta11011el/11 t1111iq11a and C. 111ar i11a (Raphidophyceae). Nippon S11i.w111 Gakkaislti, 57. 1277- 1284
[In Japanese with English summary].
34) Yamamoto. C. & Tanaka. Y . ( 1990): Two species
of harmful red tide plankton increased in f-'u kuoka
Day. 8111/. Fukuoka Prej't:CI. Fislt. Exp. So,., l6, 43- 44
[In Japanese!,
35) Yamamoto. T .. Yoshizu, K. & Tarutan i. K. (1995):
Effects of 1e111pera111rc, salini ty and irracliance on the
growth or toxic dinoflagcllatc Alexa11dri11111 wmanmse
isolated from M ikawa Bay, Japan. .lp11. J. Pltycol.,
43. 9 1- 98 [In Japanese with English su11111111ryJ.
36) Y,1mochi. S. (1984): Effects of temperature on the
grow th of six species of red- tide flagell,Hes occurrin g in Osa ka Bay. B11JI. Plank. Snc. Jpn. , 31.
15- 22 [In Japanese wi th English summary].
37) Yoshida, Y. & M iya moto. M. ( 1995): Grow th of
Heteroc11pst1 circ11larisr11111111a popula1io11 in Kusuura 13ay and variation of diurnal motion of red lide
in 1994. l<ep. K1111111111010 Prefe<'I. 1-'is/r. Res. Ce111. ,
3. J 1- 35 [In Japanese j.
( Received fo r publication. February J, 1999)