NAOSITE: Nagasaki University's Academic Output SITE
Title
The food removal rate by Noctiluca scintillans feeding on Tetraselmis
tetrathelle and Gymnodinium nagasakiense
Author(s)
Lee, Jung Keun; Hirayama, Kazutsugu
Citation
長崎大学水産学部研究報告, v.71, pp.169-175; 1992
Issue Date
1992-03
URL
http://hdl.handle.net/10069/29864
Right
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http://naosite.lb.nagasaki-u.ac.jp
Bull. Fac. Fish. Nagasaki
The
food
removal
Tetraselmis
rate
and feeds
The
secrets
food
rate
starved
4×10
about
1 × 10
-2
varied
calculated
using
the
depending
the
The maximal
rate
a model
feeding
upon
With
level
as the food
Gymnodinium
tetrathelle
feeder
The
and
level
which
clearance
experimental
increased
over
of 2-3 hour duration
was
of 4-7 hour duration
was
and that in the experiments
ml/ Noctiluca/h.
for filter
experiment.
the food
decreased
on the materials
of Tetraselmis
rate in the experimentes
ml/Noctiluca/h,
-2
its tentacle
in the suspensions
level during
T. tetrathelle,
cells/ml.
2 × 10
were
in food
Noctiluca
With
around
rates
nagasakiense
on the change
about
mucus
removal
on
nagasakiense.
scintillans
and Gymnodinium
5
Gymnodinium
feeding
HIRAYAMA
is based
duration.
and
scintillans
Jung Keun LEE* and Kazutsugu
in it.
by
by Noctiluca
tetrathelle
Noctiluca
trapped
169
Univ., No. 71 (1992)
nagasakiense,
when the experi-3
mental
and
durations
7 × 10
The
-3
were
ml/ Noctiluca/h
food
removal
increasing
food
there
no further
was
fixed
at 4 or 5 hours,
throughout
rate
levels
with
two
kinds
and,
once the maximal
increase
in spite
N scintillans
growth
words : the
Noctiluca
scintillans,
motility,
clearance
the populations
attributed
significantly
tions."'
of Noctiluca
* Graduate
a rapid
influenced
is important
their
in the
of Noctiluca.
on the
eggs
of
facts,
The
maximal
with T. tetrathelle
with G. nagasakiense.
feeding
pressure
It
on the
rate ;
Noctiluca
scintillans;
nagasakiense.
Noctiluca
mechanism,
caught
shows
a characteristic
mucoidfiltration'
in a layer of mucus
and
movement
carried
laboratory
times
secreted
longer
gradually
rate
the strings
than
the
by
the
grows
depending
of mucus."
of mucus,
the cell length
largon the
In my
several
of Noctiluca,
with algal food trapped
popula-
behavior
the role
same
trans-
Omori
and
Engineering.
The
feeding
in principle
number
in nature
as in the laboratory
and Hamner')
is
The clump of algal
and the volume
culture,
prey
around
cytostome
of the tentacle.'
food density
feeding
: The
to
cells on the tip of tentacle
a large
Science
achieved,
them.
in the material
of Marine
with
was
were often observed
(a small fish)
hatched
of these
level.
er with the enlargement
community.
School
removal
tentacle
organisms.
reduction
and Anchovy
In the light
fer of plankton
planktonic
of Noctiluca
(a copepod)
on covers
e. g., phytoplankton,
to the feeding
feeding
food
is largely vacuo-
it feeds
increased
rate
in food
considerable
Gymnodinium
and their eggs, fish eggs,
feeding of Noctiluca affects
of other
population
Acartia
which
of plankton,
protozoa,
copepods
etc.'
The voracious
rate ; the
tetrathelle;
1× 10
in nature.
(200-1000 ,um in size), has
but the food
a wide range
inflict
of G. nagasakiense
food
mg Carbon)/ Noctiluca/h
mg Carbon)/ Noctiluca/h
lated and unarmored
the
increase
algal
might
that
Tetraselmis
And
of
was
Key
diatom
of the
was about 2000 cells (or 0.75 × 10
supposed
between
the food levels examined.
and about 600 cells (or 1.5 × 10
population
Prasad2)
fluctuated
up to the maximal,
-4
little
rates
above
-4
rate
the
reported
of Noctiluca
culture.
an encounter
while
in
is the
diving
of
deep
170
LEE and HiRAyAMA ： Food Removal rate of IVoctiluca
in a lagoon： The strings of mucus extended
obtained using a haemacytometer． The food
from the cells of Noctiluca and entangled
suspensions of various food levels were made
together to from a mucus web；八「octiluca fed
by diluting the cultures with filtered sea water．
on the materials trapped in it， and， as the weight
3． Estimation of carbon contents in the algal food
of accumulating debris eventually pulled the
Hundreds ml aliquot of the food culture was
accumulation downward， they released them−
passed through the fired filter pads （GF／C）
selves from the web near the bottom， some 30
every time the food removal rate experiment
meter deep， to float individually back to the
was conducted． These samples （7 for T． tetra−
surface． Thus， the food removed by mucus is
thelle and 10 for G． nagasakiense） were dried up
not necessarily fed by Noctiluca．
at 一30 OC． After being cut into pieces， they were
The purpose of this study is to obtain
analysed for carbon contents using a C ＆ N
preliminary information on the role of Nocti−
corder （Yanako， Model MT 500）．
luca in the material transfer of plankton com−
4． Food removal rate experiment
munity． To serve this purpose， the clearance
The experiments were conducted at 230C
rates （volume swept clear） and food removal
and 22 0／oo S， the most favorable temperature
rates by the organism were obtained at various
and salinity for the growth of Noctiluca．9） The
food levels using Tetraselmis tetrathelle and
starvedハioctiluca were inoculated in the feed−
Gymnodinium nagasakiense as food organisms．
ing vessels containing various levels of food
suspensions， and allowed to remove the food
Materials and Methods
organisms for a definite period of time．
1． Noctiluca
Controls without Noctiluca were prepared to
N． scintillans was collected with a plankton
correct for the algal growth in’ 狽??@feeding
net from Nomo Bay in Nagasaki Prefecture，
vessels． The food removal rate＄ were calculated
southern Japan． lt was stock−cultured on a diet
from the number of Noctiluca， experimental
of T． tetrathelle in about 100 ml of GF／C filtered
duration， volume of food medium， and the food
seawater at 23 OC， 22 0／oo S and on 14L：10D light
concentrations at the start and end of the ex−
cycle． Experiments started two days after the
perlment．
collection and continued periodically for several
a． Experiments with T tetrathelle
months．
ハ［octiluca were starved f6r 24 hours in 500
2． Algal food
ml filtered seawater， and the aggregations
T． tetrathelle and G nagasaleiense originat−
formed on the surface were pipetted into a
ed from the stocks maintained in modified
beaker containing about 100 ml of filtered sea
Erd−Schreiber medium under the same culture
water． Special attention was paid not to give
conditions as in Noctilzaca stock culture． T．
mechanical shocks during the transfer． The
telrathelle for the experiment was grown in 500
八ioctiluca suspensions were condenSed again，
ml of GF／C filtered sea water enriched with
immediately before the experiments， into as
modified Erd−Schreiber medium （1 ： 1， volumet−
highest densities as possible （800−1000 inds．／ml）
rically）． The culture was placed in the dark
by gently pipetting out the seawater benath
for several hours and the settled down cells were
the aggregation． The density of IVoctiluca was
removed． G nagasakiense was grown in IOO ml
determined by averaging three cell counts of
of modified Erd−Schreiber medium， and the
1 ml aliquats using a chamber slide giass． One
patches formed in the culture were taken to
to five ml of this八「octiluca condensatioh were
prepare a high level of food suspension． The
swiftly transferred into the experimental flasks
conc，entrations of these cultures were deter−
containing 100 ml of food suspension． The
mined by averaging ten cell counts which were
higher the food concentration， the more
171
Bull． Fac． Fish． Nagasaki Univ．， No．71 （1992）
Btack vinyt sheet
respectively expressed as follows ：
1
Ct＝Co’ekt ・・・・・・・・・・・・・・・・・・・・・… （1），
Experimentd vessels
@ ＼
Ctf ＝ Co’e（KHf） ・・・・・・・・・・・・・・・・・・… （2），
Shqking
一＝＝向 二＝＝■ ＝二＝二一 ；＝ラ ＝＝＝
s。uching
Belt 一
一
Motor
@8
where Ct is the final food concentration in the
q。tαting
control （cells／ml）， Ctf is the final food con−
centration in the feeding vessels （cells／ml）， Co
（）＼O Speedometer
is the initial food concentration （cell／ml）， t is
the duration of experiment （hour）， k is the
Fig． 1． Schematic diagram of the apparatus used
in the feeding experiment．
growth coefficient （or specific growth rate） of
the algal food， f is the food removal coefficient
by Noctiluca．
ハioctilucα were used to produce the recognizable
Solving for k and f using equation （1） and （2），
changes in food concentration at the end of
k ＝＝ （ln Ct−ln Co）／t，
experiments． The experiments were run in
f＝ ｛（ln Co−ln Ctf）／t｝十k．
continuous dim light on an apparatus designed
The clearance rate is calculated from：
’
to assure the uniform distribution of IVoctiluca
F ＝V・f／N，
ahd algal food in the medium （Fig． 1）． A box
where F is clearance rate （ml／Noctiluca／h）， V
containing 8−10 experimental flasks was sus−
is the volume of food suspension （ml）， N is the
pended over a touching bar attatched alongside
number of Noctiluca in the feeding Vessels
a horizontal rotating axis． The box was con−
（inds．）．
tinuously shaken at a rate of six reciproca−
The mean food concentration in the feeding
tions a minuite with the maximal swinging
vessel is calculated from ：
’
distance being about 2 cm． This shaking was
C ＝＝ （Ctf−Co）／（k−f）t，
confirmed to be harmless to Noctiluca． The
where C is the mean food concentration （cell／
durations of experiment ranged from two to
ml）．
seven hours．
The food removal rate is calculated from；
b． Experiments with G nagasakiense
1一 C・F，
These experiments were run essentially in
where I is food removal rate（cells／八「octiluca／h）．
the sarne way as in the T． tetrathelle ex−
periments except that they were run statically
Results
using a smaller number of IVoctilaca in a smal−
ler amount of food suspension． Ten to fifteen
Fig． 2 shows the clearance rates by starved
八「octiluca were placed in each well of Falcon
Noctiluca at various food levels． The rates are
multiplate （＃ 3046） containing 3 ml of food
expressed by dividing them into two groups on
suspension， and the direct light was cut off by
the basis of experimental duration． The cell
covering a black vinyl sheet on the vessels． The
number was converted into carbon contents
experiments were run for four to five hours．
using the results of chemical ahalyses： the
The food concentrations were determined in the
average values of carbon contents in 1 × 108 cells
same way as in the experiments with T．
were 3．74 mg・ （S． D．： O．3） for T． tetrathelle and
tetrathelle．
25．7 mg （S． D．： 10．17） for G． nagasakiense． With
5． Calculation of food removal rate
T． tetrathelle， the clearance rates decreased as
The food removal rate was calculated using
the food concentration increased over 4×105
a model given in Ohmori and lkeda．iO） The
cells （or 1．5×10−2 mg C）／ml． Below this con−
changes in food concentration in the control and
centration， the rates in the experiments of 2」3
feeding vessels after some period of time are
hour duration were in many cases higher than
172
LEE and HiRAyAMA ： Food Removal rate of iVoctiluca
（ T． tet rdthetle ）
口
20
（ G． nag asak iense）
a
口
口
日
15
1
口
asm
10
2
■己
O
i巳10
呂層・【；li 日日
■一
ロnロ日月■
層■一
層 ■
■口
10
’
口
50
︵‘、σ噸三＝りOZ、？9×一∈︶
山之α田OZ＜￠＜山d
25
“JmZ−tuLt“
10 ． 20
2
（ceUs x104／mt）
1 10 405 10 50
（mg c xio−3imt ）
FOOD LEVEL
Fig． 2．
The clearance rates by IV． scintillans in various levels of suspensions of
T． tetrathelle and G． nagasakiense． The open squares represent the
experiments of 2−3 hour duration， and the solid squares experiments of
4−7 hour duration．
o
e
e
100
20
e
600
e
coo
e
8 ee
eeelpA e
200
・1殉●
oi
3
10 30
o
︵‘、σりコーコ。。Z、頃igxOぴ∈︶
e
@ 伽o
0 5
1
10
eeo
2、σ・コ⋮り。z企−9x・9
oi
8
9
0●●
o
00
㎜
●●
O
o
1
OO●
O 。。・9
伽
o●
︵‘、σりコ＝ぢOZ、い＝Φど
山トくに ﹂︿﹀ハ∪一≧国に ∩F∩▼∩▼L
2
o
800
︵‘、σり三一ぢOZ、gり＝Φり︶
o
oo
国トくα﹂＜＞OΣ国玉OOOL
O（5035）
ゴ
（ cetts x 1 04 1 mt ）’
O
（cetts x 104／mt）
5 10 50
1 10 50
−3
／mt）
（mg C xlO
（mgcxio−3tmo
FOOD LEVEL
Fig． 3．
The food removal rates by N． scintillans
in． various levels of suspensions of T．
tetrathelle． The open circles represent the
FOOD LEVEL
Fig． 4．
The food remov． al rates by IV． scintillans
in various levels of suspensions of G．
nagasakiense．
experiments of 2−3 hour duration and the
solid circles the experiments of 4−7 hour
duration．
those of 4−7 hour duration． The maximal value
no clear differences in the clearance rates
of the former ．w． as about 2×10−2 ml／IVocti−
between with T． tetrathelle ，and with G．
luca／h， and that of the latter， except one case，
nagasakiense．
was about 1×10−2 ml／Noctiluca／h． With G．
The food removal rates were calculated
nagasakiense， the clearance rates fluctuated
using the mean food concentrations， but plot−
throughout，the examined food level in the range
ted in Figs． 3 and 4 against the initial food
of （1−7）×10−3 ml／Noctiluca／h， and the average
concentrations as suggested by McClatchie and
rate was 4×10”3 ml／Noctiluca／h． Compared on
Lewis．ii） Fig． 3 shows the food removal rates
the basis of experimental duration， there were
with T． tetrathelle． Below 4×105 cells／ml， the
Bull． Fac． Fish． Nagasaki Univ．， No．71 （1992）
173
rate increased with increasing food levels． The
ferences between them， the maximal food re−
rates in the experiment of 2−3 hour duration
moval rates （Figs． 3 and 4） were quite different
were generally higher than those of 4−7 hour
from each other in terms of both cell number
duration， but the maximal rates were nearly the
and amounts of carbon． This is supposed to
same， except one case， at about 2000 cells （or
be due to the difference in cell size： The size
O．75×1『4mg C）／ハloctilzac〃！h． This maximal rate
of T． tetrathelle was （10L20）×20 ptm and that of
was reached in both cases around 4 x 105 cells／
G nagasaleiense was （25−30）×（28−32） ptm．
ml， and there were no further increases with
When the maximal food removal rates were
increasing’food levels． Fig． 4 shows the food
expressed in terms of cell volumes， which were
removal rates with G． nagasakiense． The rates
roughly calculated by cell length × width ×
also increased with increasing food levels， and
thickness， they were 4×10−3 mm3／Noctiluca／h
the maximal rate of 600 cells （or 1．5×10m‘ mg
with T． letrathelle and 7×10−3 mm3／IVoctilu−
C）／Noctiluca／h was reached around 1 X 105 cells／
ca／h with G． nagasakiense： The ratio of cell
ml．
thickness to cell width is about 2：3 for T
tetrathellei 2） and about 1：2 for G nagasaki−
Discussiom
ensei3）． Assuming that IVoctiluca is a ball with
a radius of 400 ptm， its volume is about 3×
The results of the experiments with T．
tetrathelle （Fig． 2） demonstrate that the clear−
10−2 mm3． and the maximal volume of food it
’
removes an hour is roughly equivelent to
ance rate is the function of both food con−
（1／8−1／4） of its volume．
centration and experimental duration． The
The maximal concentration of G． naga−
feeding of IVoctiluca in this experiment seems
sakiense in the sea reached 3×10” cells／liter，i‘）
to have occurred soon after the start of ex−
which is far higher than the concentrations
periment to see that the algal masses ap−
examined in this study． This raises a possibility
peared in the body of Noctiluca twenty minuites
that Noctiluca may inflict feeding pressure on
’after the inoculation． The food concentration
the growth of G． nagasakiense in the sea，
of 4×105 cells／ml， where the clearance rates
resulting in the suppression of red tide it
started to decline， is generally consistent with
induces． The number of IVoctiluca needed to
the concentration where the maximal growth
suppress the population growth of G． naga−
rate of八ioctiluca was obtained．9）The result that
saleiense can be roughly calculated using the
the higher clearance rates were obtained in the
following equation ：
experiments of shorter duration than in the
dC／dt ＝ k・C−F・C・N，
longer presents two possible causes． One is
where C is the concentration of G． nagasakiense
that the starved Noctiluca secreted mucus more
（cells／ml）， t is time （day）， k is the specific growth
actively in the earlier period of exposure to food
rate of G． nagasafeiense， F is the clearance rate
suspension， and the other is that they fed more
by IVoctiluca （ml／Noctiluca／day）， N is the density
actively in that period． The result in Fig． 3 that
of Noctiluca （inds．／ml）． The diel clearance rate
the maximal food removal rates were nearly
by Noctiluca will be lower than simple 24 fold
the same regardless of the experimental
of the hourly rate obtained in this study，
duration implies that the maximal rate obtain−
because Noctiluca stops feeding activity during
ed here is generally equal to the limit of food
the cell division． As it takes 6−8 hours to
removal ability in IVoctiluca． Though the
complete the cell dividioni5） and the division
clearance rates with T． tetrathelle and G．
rate also varies depending on the environmental
nagasakiense， when compared on the basis of
experimental duration， showed no clear dif一
conditions9＞． the diel rate in this calculation was
’
assumed to be about ten fold of the hourly rate．
174
LF．E and HiRAyAMA ： Food Removal rate of IVoctiluca
Taking as an example F ＝ 4× 10−2 ml／IVoctiluca／
perimental induction of feeding behavior in
day， k ＝ O．7 （G． nagasakiense divides nearly one
IVoctiluca miliaris， Protoplasma， 125， 34−42．
time a day in the laboratory culture）’6’， C ＝ 5×
8） Omori， M， and W． M． Hammer （1982）：
104 cells ／ml， 18 Noctiluca／ml will be needed to
Patchy distribution of zooplankton ： behav−
stop the population growth of G， nagasafeiense．
iour， population assessment and sampling
But， as this study was conducted under constant
problems． Mar． Biol．， 72， 193−200．
environments in the laboratory， confirmative
9） Lee， J． K． and K． T． Hirayama （in this is−
field studies are necessary to apply the results
sue）：The effects of salinity， food level and
obtained here to the phenomena occurring in
temperature on the population growth of
nature．
八ioctiluca scintillans（Macartney）．
10） Omori， M． and T． lkeda （1976） ： Methods of
References
Zooplankton Ecology，＊’ts Tokyo： Kyoritsu
syuppan． 128−129．
1）
2）
3）
4）
5）
6）
7）
Enomoto， Y． （1956） ： On the occurrence and
11） McClatchie， S．， and M． R． Lewis （1986）：
the food of Noctiluca scintillans （Macartney）
Limitations of grazing rate equations ： the
in the waters adj acent to the west coast of
case for time−series measurements． Mar．
Kyushu， with special reference to the
Biol．， 92， 135−140．
possibility of the damage caused to the fish
12） Okauchi， M． N． （1988）： The mass culture
eggs by that plankton． Bull． Jap． Soc． Scien．
and food value of Tetraselmis tetrathelle．＊＊
Fish．， 22， 82−89．
Saibai Giken， 14（2）， 85−110．
Prassad （1958）： A note on the occurrence
13） Takayama， H． and R． Adachi （1984） ： Gymno−
and feeding habits of Noctiluca and their
dinium nagasakiense sp． nov．， a Red−tide
effects on the plankton community and
forming Dinophyte in the adj acent waters
fisheries． Proc． lndian Acad． Sci． Sect． B 47，
of Japan． Bull． Plankton Soc． Japan， 31（1），
331−337．
7−14．
Hattori， S． （1962）： Predatory activity of
14） Matsuoka， K．， S． lizuka， H． Takayama，’
IVoctiluca on Anchovy eggs． Bull． Tokai Reg．
T． Honjo， Y． Fukuyo． T． and lshimaru （1989）：
Fish． Res． Lad．， 9， 211−220．
Geographic distribution of Gymnodinium
Sekiguchi， H． and T． Kato （1976） ： lnfluence
nagasaleiense Takayama et Adachi around
of IVoctilzaca ’s predation on the Acartia pop−
west Japan． Red Tides： Biology， Envi−
ulation in lse Bay， central Japan． J． Ocea−
ronmental science， and Toxicology， Edit．
nogr． Soc． Japan， 32， 195−162．
Okaichi， Anderson， ＆ Nemoto， Elsevier sci．
Uhlig． G． and F． Sahiling （1985） ： Blooming
pub． Co．， 101−104．
and red tide phenomenon in Noctiluca
15） lshikawa， C． （1894）：Studies of reproductive
scintillans， lnternational Symposium on
elements． II．八roctiluca miliaris Sur．・Its
Marine Plankton． Shimizu （Japan）． 22， Jul
division and spore formation． J． Cell． Sci．
−1， Aug，， 779−780．
Imp． Univ． Tokyo， 6， 297−334．
Metivier， C． and Soyer−Gobillard， M． 一〇．
16） lizuka， S． and K． Mine （1983）： Maximum
（1986） ： Motility of the tentacle of Noctilaca
Growth Rate of Gymnodinium sp． （Type一
scintilans Macartney， a highly evolved dino−
’65）， a． Red Tide Dinoflagellate， Expected
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under Culture Conditions．＊ Bulletin of
（2）， 163−170．
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＊ ： in Japanese with English summary
＊＊ ： in Japanese
’
Bull. Fac. Fish. Nagasaki
夜光 虫 (Noctiluca
Gymnodinium
scintillans)
nagasakiens
李
Univ., No. 71 (1992)
の Tetraselmis
175
tetrathelle
と
懸濁液 中での餌料 除去率
正根 ・平 山
和次
夜光 虫は触 手 の周 りに粘 液 を分泌 して餌 料 を集 め摂 取 す る 。炉 水摂 餌 す る生 物 に用 い られ る
餌 料密 度 の減 少 か ら間接 的 にそ の摂 餌量 を求 め る方 法 を応 用 して,い ろ い ろな 餌料 密 度 あ る い
は摂餌 時 間で 夜 光 虫を飼 育 し,そ の餌 料 密度 の減 少 か ら,み か け の戸 水速 度,餌 料 除 去速 度 を求
めた 。 T
tetrathelle
を餌 料 とす る と,餌 料 密 度 が 4 × 10' cells/ml
(2-3時 間)で 求 めた 最高 炉 水速 度(約 2 × 10'
ml/ Noctiluca/h)
めた ものほ ぼ2倍 で あ った 。餌 料 密 度 が 4 × 105cells/ml
G. nagasakiense
Noctiluca/h
以 下 の時,短 い 実験 時 間
は長 い 実験 時 間(4-7時 間)で 求
以上 で は炉 水 速 度 は低 下 した 。 ま た
を餌 料 と した 時(実 験 時 間 は4-5時 間),炉 水 速 度 は
1×IO-3と7×10"3ml/
の間 で変 動 した。 どち らの餌 料 の場合 で も餌 料 除 去速 度 は餌 料 密 度 の増 加 と とも
に 増加 し最 大値 に達 した 。 それ 以 上 の餌 料 密 度 で は餌 料 除去 速 度 の増 大 は 認 め られ な か っ た。
最大餌 料除去速度は T. tetrathelle
の 場 合 は 2000 cells
(また は 0.75 × 10'
mg Carbon)/
の場 合 は 600 cells (また は 1.5 × 10'
mg Carbon)/
Noctiluca/h
で あ り G. nagasakiense
Noctiluca/h
で あ っ た 。海 域 で夜 光 虫の 密 度 が高 い場 合 には,そ の摂餌 が G. nagasakiense
増殖 を抑 制 す る 可能 性 は 充 分考 え られ る。
の