The in situ growth rates of some deep-living oceanic dinoflagellates:
Pyroc ystis f usif ormis and P yroc ystis noctilucal
Elijah Swift, Marc Stuart”, and Valerie
Graduate
School of Oceanography,
University
Maunier
of Rhode
Island,
Kingston
02881
Abstract
Division rates of Pyrocystis spp. were estimated for natural populations
by determining
the proportions
of dividing cells produced each day. In Mona Passage (West Indies ), P.
fusiformis
and P. noctiluca
appeared to divide fastest at 80-100 m, the depth of their
maximum cell concentration.
Pyrocystis noctiluca divided at about the same rate in the
mixed layer as in the. thermocline,
while P. fusiformis
divided much more slowly in the
stages of both species were negatively
mixed layer than below. In culture, reproductive
buoyant, but vegetative
cells were positively
buoyant.
The effect of such buoyancy diffcrences (and the rising and sinking rates which result from them) on the estimation of
natural division rates was apparently negligible in the mixed layer and of some importance
in the more stable waters of the thermocline.
Pyroccystis noctiluca and P. fusifmnis are
oceanic dinoflagellates common to regions
whcrc surface Gnmcratures are above 20°C
and seawattir is indiluted
by land runoff
(Taylor 1973). D uring the asexual reproduction cycle of these species, morphologically distinct reproductive bodies develop
within the parent cell wall. Usually two
reproductive
bodies are formed, but instances of single reproductive body formation are not uncommon (Swift and Durbin
1971). The frequency of n&w cells produced daily in a natural population, the
“percent daily augmentation” ( Gran 1912))
can be estimated from the frequency of cells
containing
two re’productivc
bodies. In
this way we have estimated doubling times
for populations of Pyrocystis species within
the mixed layer ( Swift and Durbin 1972).
At a station in the equatorial Pacific
Ocean with only lo-15 m of superficial
wind-mixed layer, Sukhanova and Rudyakov ( 1973) found that the mean depth of
vegetative cells of P. noctiluca was ca. 70
m while that of cells containing rcproductivc bodies was ca. 120 m. They suggest&d
that if the reproductive state was accompanied by an increase in density, acccler1 This work was supported by funds from the
Oceanography
Section of the National
Science
Foundation
( grant GA30893h).
Columbus
Labora’ Present address : Battelle
tories, William F. Clapp Laboratories,
Inc., Washington Street, Duxbury,
Massachusetts
02332.
LIMNOLOGY
AND
OCEANOGRAl’IIY
ated sinking of the reproductive cells could
explain the vertical separation of the two
cell types. They also noted that if the reproductive process took place within a period
of several hours, as they expected, the sinking rates of the reproductive cells would be
unusually fast for cells of their size (Smayda
1970). IIerc, we have used laboratory cultures to cstimatc sinking rat& of different
stages in the cell cycle. In addition, we
have extended our studies to depths OF 200
m, below the’ mixed layer, and examined
some field populations to see to what cxtent a vertical displacement of vegetative
and reproductive cells might affect our cstimates of in situ division rates.
Methods
De tails of the isolation and culture of
Pyrocystis fusiformis
Murray in Murray
and Thomson and Pyrocystis noctiluca Murray in Murray and Thomson will be given
elsewhere ( Bhovichitra and Swift in prep. ) .
All culture’s were grown in Sargasso Sea
water enriched as in the Guillard and Ryther ( 1962) f/2 formula, but without added
silicon, at room temperature ( ZO-25OC) beside a north window or in a temperaturccoutrollcd light chambkr at 22°C under
“cool-white”
fluorescent lamps at about
7,000 lux on a 12 : 12 LID cycle.
To determine if cells were negatively or
positively buoyant, we counted a sample
418
MAY
1976,
V. 21(3)
In situ growth
drawn from a well stirred culture flask and
introduced
into a l-cc Sedgwick-Rafter
chamber. After 5 min, cells found at the
top of the chamber were considered to be
positively buoyant, those at the bottom of
the chamber negatively buoyant. Sinking
rates of negatively buoyant cells were detcrmined by the inverted microscope technique described by Smayda and Boleyn
(1965).
Field samples were collected on RV Trident cruises 109 (3-18 January 1972)
and 129 (17-31 January 1973) in Mona
Passage, between Puerto Rico and Hispaniola. In 1972, the sampling was mainly
within the mixed layer, ca. 6 km west of
Rincon, Puerto Rico. In 1973, a buoy with
drogues to 150 m was launched ca. 25 km
north of Mona Island and this drifting buoy
was used as a reference point for net tows
and samples. Hydrographic
data on both
cruises were obtained from Niskin bottle
casts. Hydrolyzable
and inorganic phosphate were determined by the methods dcscribed by Strickland and Parsons ( 1968))
ammonia by the Solorzano (1969) method,
an d urea by the method of McCarthy
( 1970). Light extinction was determined
with a submarine photometer and insolation
was measured by integrating the recorded
signal from an Epplcy model 548 pyranomcter. In 1972, net tows were made in the
mixed layer using TSK-flowmeters on open
0.5-m nets of 25- or 65-pm porosity. During 1973,0.5-m nets of 65- or 180~pm porosity with TSK-flowmeters were used to sample to 200 m. Tows were made for at least
20 min at about 2-4 knots.
Estimation of the potential daily increase
in the population was calculated on the
basis of each day’s observations of the frequency, a, of cells containing two reproductive
bodies within
the population
samples. From a, the percent daily augmcntation, the extrapolated rate of increase
in cell number is given by the formula
N = N,( 1+ a)Y’,
where N is the potential number of cells
found after an integral number of days, T,
have elapsed since the cell number was No.
419
rates
c
50r----x7
SUNSET
EASTERN
STANDARD
TIME
Fig. 1. Percentage
of different
reproductive
stages in a culture of Pyrocystis noctiluca grown
by a north window.
Negatively
buoyant
cells
with one (---O---)
or two (-•-)
reproductive
bodies were found at the bottom of
the chamber, as were the newly formed vegetative
cells (-A). Later, the new vegetative
cells
became positively
buoyant and were found at the
top of the counting chamber (---A--).
The production of new cells is confined to
the early morning hours. The formula predicts a stepwise increase in cell number.
Results
Buoyancy changes associated with the
Ztfe cycle-The
vegetative cells of these
species are usually positively buoyant in
culture. The reproductive stages and newly
formed vegetative cells of cultures grown
by the north window were found to be
negatively buoyant (Figs. 1 and 2). New
vegetative cells developed positive buoyancy about 6 h after their formation. The
time during which cells with completed rkproductive bodies were present was 23000900 for P. fusiformis and 0200-0400 for ‘P.
noctiluca. A similar interval was reported
earlier for P. noctiluca in nature (Swift and
Durbin 1972). These field and laboratory
data indicate a period of about 18 h during
reproduction
when cells would be negatively buoyant. However, cells in culture
sometimes became negatively buoyant before the final reproductive stages, and the
time over which negative buoyancy extends
probably varies with growth conditions,
420
Swift
- --I__----. -- -----_ -- .-_
4
7--_I GHTS’
OFF
A..
LIGHTS
ON
PYROCYSTIS
FUSIFORMIS
LIGHT:
et al.
Table 1. Sinking rate of Pyrocystis
noctiluca
and Pyrocystis ftrsifotmis
as measured in a settling
chamber.
A
.
Species
Cell
Type
\
Bi
%Z%ik
EASTERN
STANDARD
TIME
Fig. 2. Percentage
of different
reproductive
stages in a culture of Pyrocystis fusiformis
grown
by a north window.
Symbols as in Fig. 1. New
vegdative
cells could not bc distinguished
from
0th
vcgetativc
cells after 1800 hours ( 12 : 12
LI> cycle).
For example, in one instance a large numher of cells of P. noctiluca, with bilobate
protoplas ts ( a stagc preceding caryokinesis ) were observed to be ncgativcly buoyant
and remained so for at least 3 days until
undergoing the final stages of reproduction,
Cells of P. fusiformis with bilobatc protoplasts were obscrvcd to become negatively
buoyant at least a day before they formed
reproductive bodies.
The rates at which cells from cultures
sank in a settling chamber are given in Table 1. Formalin-preserved
cells sauk at the
same rates as cells with reproductive bodies,
implying
that, in contrast to vcgetativc
cells, mature reproductive
cells maintain
no control of their buoyancy. Cells of P.
noctihca and P. fusiformis with bilobatc
protoplasts did not sink as fast as cells with
completed rep toduc tive bodies.
Augmentation
of P. noctiluca in the
<mixed Zayer-In January 1972, four to six
tows were taken between midnight and
sunrise with the net being pulled up and
down between the sea surface and the top
of the thermocline. Hydrocas ts for nutrient
data were taken each day between 0200
and 0400. The daily percent augmentation
of P. noctiluca from such tows for the entire mixed layer is given in Table 2 along
with associated nutrient data, daily insolation, and typical wind speed values. The
lobate
Sinking
Rate
(m/day)
2.6
Reproductive
14-18
Bilobate
4.0
Reproductive
14-17
mean value of augmentation found over 4
days was 8.5% and this corresponded to an
extrapolated doubling time for the population of ca. 8.5 days. A doubling time of 3.5
days is typical oE P. noctiluca dividing at
maximum rate in laboratory culture (Swift
and Meunicr 1976). As in a previous study
(Swift and Durbin 1972)) the division rate
of the cells appcarcd to be rather steady
over a prolonged period, here of 4 days.
The cell concentrations reported in Table
2 were based on pairs of nets with flowmeters. One net was positioned at 10 m,
the second at 5-10 m above the top of the
thcrmoclinc.
Cell concentrations should be
considcrcd approximate as flowmeters were
not recalibrated during the cruise.
Vertical profiles of augmentation and cell
concentrations in Mona Passage-During
25-28 January 1973, net tows were made
at six depths to 200 m four times a day to
estimate the vertical distribution
of ccl1
numbers and daily augmentation (Figs. 3,
4, and 5). If during the slowest tows at 2
knots, for the standard 20 min, the nets
passed through about 1,200 m of water,
then as they were lowered to depth and
raised to the surface they would pass
through a distance of cc?. 400 m for a 200
13-1tow, 300 rri for a 150 m tow, etc. In estimating the effect of contamination of samples by cells from shallower depths, ‘WC
could not prove significant cell populations
of P. fusiformis and P. raoctiluca existed below 150 m (Figs. 3 and 4). Even with COIItamination, it is still clear that the maximum number of cells of P. fusiformis and P.
In situ growth
421
rates
Table 2. Daily augmentation
of Pyrocystis noctiluca
populations
in the mixed layer based on a
series of 2-4 net tows taken from 0100-0400 hours bctwecn the sea surface and the thermocline,
Ancillary information
on nutrient concentrations,
insolation, and typical wind speeds are given. Augmentation and nutrient values are for predawn of the day indicated;
insolation was recorded in the subsequcnt daylight period.
Temperature
and salinity in the mixed layer were 26°C and 36.5%.
-14 Jan
Depth,
m
NH3
1972
Urea
(PM)
15 Jan
PO4
NH3
1972
Urea
(vM)
1G Jan
PO4
5
0
0
0
0
0
0
Org.
P
NH3
1972
Urea
(IJM)
0.02
0
0
17 Jan
PO4
NH3
0
0
1972
Urea
CUM)
PO4
0
0.01
50
0
0
0
0
0
0
0
0
0
0
0
0
80
0
0
0
0
0
0
0.02
0
0
0
0
0
140
0
0
0.04
0
0
0.10
0.07
0
0
0.07
0
0
0.10
200
0
0
0.17
0.15
0.1
0.28
0.09
0
0
0.32
0
0
0.28
Augmentation
Cell
Cont.
Augmentation
= 7.7%
= 100 ms3
Insolation
= 12.3
Wind
Speed
= 30 km h -'
Mixed
Layer
Depth
x lo6
Cell
J/m2
= 80 m
Cont.
Insolation
= 9.5
Wind
Speed
= 15 km h ml
Mixed
Layer
noctiluca occurred at about
the top of the thermocline.
formis population stems to
in bulk to grentcr depth than
of P. noctiluca (Figs. 3 and
25
I
Augmentation
Depth
x lo6
Cell
J/m2
= 70 m
70-80 m, near
The P. fusihave extended
the population
4). The prtis-
CELLS,
0
= 8.0%
= 52 ms3
m-3
Augmentation
= 10.3%
Cont.
Cell
= 82 Inm3
Insolation
= 12.6
Wind
Speed
= 8 km h ml
Mixed
Layer
Depth
x lo6
J/m2
= 70 m
= 58 lms3
Insolation
= 16.2
x lo6
Wind
Speed
= O-6
km h -'
Layer
Depth
Mixed
J/m2
= 80 m
encc of contamination
also suggests that
thcrc may bc no value of augmentation
greater than zero much below 100 m for
P. noctiluca (Figs. 4 and 5) or below 150
111for P. fusif ormis ( Figs. 3 and 5). The
valu& of augmentation for tows taken at
150 m or below is very close to that cx-
50
I
CELLS'm-3
0
a
50
l
I------
l
m
l *
l
e
'
l
l
le
E
.a 100
l
I
.
200
I
150
I
l
t
z
W
100
P
50
Fig. 3. Cell concentrations
of Pyrocystis fusifrom open metered net tows ( 0 ) arc not
corrected for contamination
(see text).
Mean cell
concentrations
at standard
depths
(-•--)
were interpolated
from pairs of values above and
below the depths, Mona Passage, 1973.
= 7.9%
Cont.
0
l
PYffocYsr/s
NOCTILUCA
:
forntis
1
Fig. 4. Ccl1 concentration
of Pyrocystis noctiZuca, Mona Passage, 1973. Details as in Fig. 3.
422
Swift
et al.
Pyrocysfis
nod
ihca
DEPTH,m
5
I
09
IO
I
0
IO
I
26 Jan ‘73
27 Jck73
I
I
5
k&l
I
*O”O
I
IO
1
I 1
I
I
L--L---IO
b3
20
40
60
I
I
DA;LY
PEROCENT5
&MEbiTATbN
Pyf ocysf is
fusiformis
DEPTH.m
20
I
40
I
0
27 Jan’73
28 Jan’73
T
2001 /
0
I
A;OLY
D
I
40
I
PEROCENT20
A;GME&ATl%d
40
60
Fig. 5. Daily percent augmentation
of Pyrocystis fusiformis
and Pyrocystis noctiluca as a function
of depth iu Mona Passage, 1973. Values are based on tows made with open nets; values greater than
zero below about 150 m appeared to be due to contamination
(see text). Augmentation
based on single net tows is given as a most probable value ( @ ) and the brackets are 95% confidence limits on the
counting error. The percent augmentation
scale ranges from O-6070 for P. fusiformis
and O-15%;, for
P. noctiluca.
In situ growth
Table 3.
tis fusiformis
Vertically
integrated
values of daily percent augmentation,
and Pyrocystis noctiluca in Mona Passage, 1973.”
Species
Depth
Interval
(meters)
Pyrocystis
fusiformis
O-70
75-200
p;;;;r;,';;
423
rates
a, for populations
Days to Double
Population,
Mean (Range)
Mean Value
of a
26 Jan
7.45
12
27 Jan
5.7
28 Jan
(%I
4.95
6.0
of Pyrocys-
12 (10-14)
21
21
18
4 ( 4- 6)
17
16
16
5 ( 4 -7)
O-200
10.5
O-70
3.9
3.0
5.9
4.3
16 (12-23)
75-200
3.25
5.0
7.0
5.1
14 (10-22)
3.5
4.2
6.6
4.8
15 (11-20)
O-200
*Submarine
photometer
and the 0.1% isolume
readings
indicate
the 10% isolume
at 40 m, the 1% isolume
at 80 m,
at 120 m. Insolation
on 26 Jan was 13.5 x 106 J m-2 and on 27
Jan, 13.0 x 106 J m-2. The 25th of Jan was similarly
bright
sunny day.
Typical
wind
speeds were 8-16 km h -1 in the morning and 24-32 km h -1 in the afternoon
and evening.
petted from collecting cells only when the
net is lowered and raised, with none collected below 150 m; i.e. the apparent valucs of augmentation at 150 to 200 m are
similar and almost identical to that value
of augmentation integrated from O-200 m
(see helozu, Table 3, Fig. 5). Associated
hydrographic data are shown in Fig. 6.
The data in Fig. 5 do not nticessarily indicate that Pyrocystis spp. were growing
at the depths where the augmentation was
measured, even if the results were not obscured by contamination.
There might
have been a vertical separation of vegetative’ populations from the denser reproductive stages they produce. To account for
any vertical separation of the two cell types,
WC determined the value of p&cent augmentation for the two Pyrocystis populations per unit area for the depth ranges O70 m ( mixed layer ) , 70-200 ( thtirmoclinc) ,
and O-200 m using the data in Figs. 3, 4,
and 5. These values are given in Table 3.
The most striking result is the contrast bctwccn thd two species. In general, P. noctiZuca divided about as fast in the mixed
layer as below it, while P. fusiformis divided much faster below the mixed layer.
Size distribution
of cells with depthCells collected at different depths were
measured. Vegetative cells of P. noctiluca
d&creased in size below the mixed layer,
while P. fusiformis showed no consistent
decrease (Tables 4 and 5).
Discussion
The contribution
of the two species of
Pyrocystis to the primary productivity
of a
nM
NO,
200
I
nM
4
0
tNO,-a
400
I
600
I
600
I
PO4
100
-0
150
200
50
E
Il-
100
a
W
0
150
200
_20
22
24
DEGREES
26
26
30
C
Fig. 6. Hydrographic
data taken from a bottle
cast and an expendable
bathythermograph
trace
in Mona Passage, 26 January
1973, near the
drogue used as a marker for net tows.
424
SWift et al.
Talk
4. Measurements
of the diameter
of
V~.lrocz&~ noctiluca cells as a function of depth,
Mona Passage, 0200-0400 hours, 28 January 1973.
Tow Depth
04
Cell
Mean
---
Diameter,
+S D
pa
595%
CL
Table 5. Measurements
of the length
and
width of Pyrocystis fusifomis
cells as a function
of depth, Mona Passage, 0200-0400
hours, 28
January 1973.
-------_---_---______
-- ___
-Depth
(m)
Length
i
95X C L
Width
pm
________~
-
25
447
119
21
47
399
112
19
74
347
120
16
95
363
122
21
142
351
119
21
172
-------_____
351
113
20
_ -----___
region like Mona Passage appears to bc
rather small. .Both species together contribute about 0.1% of the primary productivity. To estimate this contribution,
we
used the formula
% primary
prod.
(cells mm-“)(a d-l) (g C cell-I)
~- --- -.
(total primary prod., g C m-” d-r)
Values of cellular carbon were taken from
laboratory data (Swift ct al. 1973), ccl1
concentrations
from the data presented
hcrc for 1973, and total primary productivity From Ryther’s (1963) estimate for the
open ocean of ca. 50 g C m-” yr-I. We used
vertically integrated values of a from Table 3 of 15% cl-l for P. fusiformis and 5%
d-l for P. noctiluca.
In Mona Passage, the population maximum of P~rocys~is species seemed to bc
near the 70-80-m depth; in general, they
may bc thought of as relatively deep-lying
species. Although Apstein’s (1909) counts
indicated that more P. noctiluca and often
more P. fusiformis were found below 200 m
than above it, the work of others suggests
that ( as in our study) population maxima
near 100 m arc more common ( Karstcn
1907; Gaardcr 1954; Wood 1966; Sukhanova
1973; Sukhanova and Rudyakov
1973).
Pyrocystis noctiluca was the deepest lying
of the five common tropical dinoflagellate
species studied by Sukhanova ( 1973).
.! 95% C L
1ill1
--
~-.-
2s
1096
i
59
230
i
47
1062
c 47
191
c 27
37
74
1083
iz 65
171
+ 27
95
1033
2 76
162
A 14
142
953
L 80
213
t
172
1006
+ 67
192
? 27
_--
27
--_-
The vertical profiles of in situ division
rates taken at fact value suggest that P.
noctiluca, and especially P. fusiformis, divide fastest within
the thermocline,
at
depths of 80-100 m. The division rates
found at 80-100 m are as fast as those measured in laboratory cultures under optimum
conditions (Swift and Mcunier 1976). The
slower division rates observed in the mixed
layer might be due to nutrient limitation or
to the photoinhibitory
cffccts of high light
intensity on nutrient dcpletcd cells. An alternate explanation for the low percentage
of rcproductivc
stages in the mixed layer
would be that they are denser than the
vegetative stages that produce them and
may tend to sink out of the mixed layer
and not be counted. Such a density dependent depletion of reproductive
cells
seems mllikely
( Stommel 1949; Smayda
1970). IF we assume that convection cells
in the mixed layer are wind driven (but
see Faller 1971)) and that downwelling
(or
upwelling)
velocities arc a’bout 1 cm s-l
for each m s-l of wind speed (Scott ct al.
1969), then convection cell speeds in 1.972
ranged from 100400 m h-.r preceding the
midwatch tows, and, in 1973, they were
about 300 m h-L. On the basis of Stommel’s
concept of rctcntion times, these mixing
speeds suggest that rather complete suspension and mixing of vegetative and reproductive
cell stages occurred in the
In situ growth
mixed layer, as the densest reproductive
stages would sink at a rate of only 0.6 m
h-l in still water.
In the thermocline, where vertical mixing
is much less intensive than in the mixed
layer, there may be some vertical displacement of vegetative and reproductive cells
such as that observed by Sukhanova and
Rudyakov ( 1973). Our experimentally dctermined sinking rat& for reproductive
cells in cultures (Table 1)) coupled with
the duration of the stages (Figs. 1 and 2))
would not stem to permit more than about
a 10-20-m descent of the reproductive
stages relative to the depth they occupied
as vegetative cells. However, cells in early
stages of reproduction
(with bilobate protoplasts), which are often negatively buoyant in culture, might sink in the field for
a number of days at about 2-4 m d-l (Table 1). In Mona Passage, the generation
time of P. noctiluca of 15 days in 1973
would permit some accumulation of rcproductive stages at depth, but for this species
the value of augmentation is rather constant with depth. In contrast, P. fusiformis
showed a marked increase in reproductive
cells with depth, but the generation time of
4-5 days would not allow time for extensive vertical migration of reproductive cells.
We found complete or nearly complete r&
productive
stages only in our midwatch
tows, and not in our morning, afternoon,
and evening tows. Thus we are sure that
they were formed each day and do not rcpresent a persistent accumulation at depth
of nonfunctional
or long-lasting rcproductivc cells. Sukhanova and Rudyakov (1973)
did not mention diel pcriodicity in the occurrence of cells with two reproductive
bodies, although they made their tows at
ca. 2 h intervals for nearly a day.
Submarine photometer lowerings in 1973
placed the 1% isolumc at about 85 m, but
this green-sensitive instrument, while adcquate for coastal work, underestimates the
depth of penetration of the predominantly
blue light as a quantum flux in clear occanic waters, so that the compensation
depth is some 30 m deeper (J. Yodcr personal communication).
A 1% isolume was
rites
425
defined by a photometer at 85 m in the
clear waters of Lake Tahoe, California, by
Kicfer et al. ( 1972). They found net primary production to go to zero between 100
and 150 m as we did here for cell division.
The results from laboratory expcrimcnts on
light response arc in agreement with these
field observations
( Swift and Mcunier
1976). Both species grow particularly well
at low light intensities, although their compensation intensity is not lower than that
of other algae examined. Using the surface
irradiance of about 12 X 10” J m-2 d-’ and
assuming Jcrlov (1968) type I water, we
calculate the division rate of the species to
bc maximal at ca. 70 m, half-maximal at
80-90 m, and at compensation at ca. 100 m.
In the present study, little diminution in
cell size with depth was noted. A marked
pattern of decreasing cell size in response
to decreasing light intensity has been found
in laboratory cultures, particularly with P.
fusiformis (Swift and Meunicr 1976). The
field results suggest either that the cell
populations arc mixing vertically on a time
scale shorter than the month or more it
would take for thd population size to dccrease, or that other factors besides light
intensity affect ccl1 size as a function of
depth in the field.
References
APSTEIN, C. 1909. Die Pyrocysteen
dcr Plankton-Expedition.
Ergeb.
Plankton
Expect.
Humboldt
Stilt. 40: l-27.
F'ALLER, A. J. 1971. Oceanic
turbulence
and
the Langmuir circulations.
Annu. Rev. Ecol.
Syst. 2: 201-236.
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Submitted: 2 September 1975
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