EFFECT OF LIGHT INTENSITY
ON PHOTOSYNTHESIS
BY THERMAL
ALGAE ADAPTED TO NATURAL
AND REDUCED
SUNLIGHT1
Thomas D. Brock and M. Louise Brock
Department
of Microbiology,
Indiana
University,
Bloomington
47401
ABSTHACT
Thermal algae in alkaline hot springs of Yellowstone
National Park (Wyoming)
grow as
compact mats in which self-shading is extensive, as shown by measurement by autoradiography of photosynthetic
activity of cells at different
levels in the mat. The effect of light
intensity on photosynthesis
of the algal mats was studied using neutral density filters during
incubation
with l”CO
Despite the intense sunlight at the altitude of Yellowstone,
light
inhibition
by full sur$ght was observed only occasionally;
the rate of photosynthesis
fell
progressively
with decreasing light, although the most efficient use was at 7-14s
of full
sunlight.
Later, the light intensity over portions of the algal mats was reduced to 18% of
full sunlight by installing neutral density glass plates, and changes of chlorophyll
content,
cell number, and response of photosynthesis
to light intensity were determined
over the
next year. Although the chlorophyll
content of the algae at the surface of the mat rose
quickly,
the chlorophyll
content of the mat as a whole rose slowly or not at all; the
photosynthetic
response of the algal mats to full and reduced sunlight also changed slowly
or not at all. Although individual
algal cells can adapt rapidly to changes in light, the
entire population,
because of its existence in compact mats, adapts slowly. At the latitude
of Yellowstone there is sufficient light throughout
the year to enable algal growth to occur
even at temperatures near the upper limit at which blue-green algae can grow; in Iceland,
hot spring algae cannot grow during several winter months. Natural ultraviolet
radiation
neither inhibited
nor stimulated photosynthesis.
shaped forms usually classified in the
( Copeland 1936).
The relationship
of photosynthesis
to genus Synechococcus
We
have
described
elsewhere
(Brock and
light intensity in natural algal populations
Brock 1967) methodology for measuring
is of considerable theoretical interest. Earphotosynthesis of hot spring algae by the
lier work has made USC either of natural
14C method. Since the water column over
populations for which the previous light
the algal mats is shallow (14 cm) and
regime had not been controlled (Goldman,
Mason, and Wood 1963; Stepanek 1965; because of the altitude and climatic conditions at Yellowstone, the algae are often
Rodhe 1965) or laboratory cultures (Jorgenexposed to high light intensities, noontime
sen and Steemann Nielsen 1965; Yentsch
and Lee 1966; Brown and Richardson 1968) values of over 1.3 g cal cm-2 min-l being
for which light intensities as high as those rather frequent. By use of neutral density
filters it is possible to reduce the light
frequently
found in nature are difficult
intensity during 14C incubation experimento obtain.
tally and hence to define the response
This paper describes a series of experiments on the effect of light intensity on of the algae to different intensities. It is
also possible to study the rate of adaptanatural algal populations
in a thermal
tion
of the algae to an experimentally
respring in Yellowstone National Park (Wyo,duced light regime under conditions where
ming),
In the temperature range used,
light is essentially the only variable.
the only algae present are unicellular rodThe current study extended over three
1 For the purposes of this paper, “light”
is consummers and two winters and was supstrued to include all wavelengths
of electromagported by National Science Foundation
netic radiation
to which
the Kipp and Zonen
Grants GB-5258 and GB-7815 and in the
solarimeter
is sensitive.
No psychophysical
conlater stages by U.S. Atomic Energy Comnotation is implied.
334
INTRODUCTION
l?IIOTOSYNTHESIS
BY
mission Contract COO-1804-7. T. D. Brock
was a Research Career Development
Awardee of the U.S. Public Health Service.
Some of the winter observations were carried out while T. D. Brock was a member
of Yellowstone Field Research Expeditions
directed by Dr. V. Schaeffer and supported
by the National Science Foundation.
The
cooperation of Mr. J. Good and Dr. J.
Douglass of the National Park Service is
gratefully acknowledged. This work benefited from the able technical assistance of
S. and J. Murphy, P. Hollernan, and T.
Daley.
METIIODS
All experiments were done with algal
mats growing in the effluent channel of
Mushroom Spring, a large alkaline spring
in the Lower Geyser Basin of Yellowstone National Park. Thermal and chemical characteristics of this spring have been
described ( Brock 1967a, b) .
Methodology for quantification
o,f chlorophyll and photosynthesis has been described (Brock and Brock 1967). In the
current work, the 0.28cm2 cores used for
isotope studies were placed in s-ml screwcapped vials. NaH14C03 with a specific
radioactivity
of 10 @i/l00
pg was used
at a final concentration in the vials of 0.1
pCX/ml, except in the autoradiography
experiments where 1 &i/ml
was used.
Temperature was measured with thermistors, which were checked occasionally
against mercury thermometers.
Incident radiation was measured with a
Kipp and Zonen solarimeter (Delft, Holland) connected either to a Keithley electrometer or to1 a Cole-Parmer Mark VII
recorder. According to the manufacturer,
the solarimeter produced 8.8 mv when
receiving 1 g cal cm-2 min-l radiation. For
winter studies, light was measured with a
hand-held Gossen Super Pilot light meter
using an incident light attachment and the
readings converted to light intensity using
a calibration
curve given by the manufacturer. The light meter previously had
been checked against the solarimeter and
was reasonably accurate. The light intensities listed for the experiments represent
THERMAL
335
ALGAE
integrated values for the periods of incubation with radioisotope.
To reduce light intensities during imubation with isotope, nylon mesh fabrics
were used. The light reduction by various fabrics was measure,d using a Westotn
foot-candle meter. The per cent transmission of the fabrics was the same on a
bright clear day (8,000 ft-c) as on a cloudy
day (3,090 ft-c). The absorption spectra
of the nylon fabrics were completely flat
over the range from 760 to 320 nm. After
calibration, the fabric was sewn into small
bags that accepted snugly the s-ml vials.
Bags providing
70% transmission
were
made using two layers of white nylon chiffon ( Sears, Roebuck and Co.). Black nylon chiffon ( Sears, Rolebuck and Co.) was
used for the other bags as follows:
44%
transmission, 1 layer; 14% transmission, 2
layers; 7% transmission, 3 layers. The
bags were color coded during, manufacture.
To achieve complete darkness, vials were
wrapped in aluminum foil.
Methodology for cell counting and autoradiography
has been described (Brock
and Brock 1968a, b ) .
RESULTS
Effect
of natural ultraviolet radiation
on photosynthesis
It is well known that natural ultraviolet
radiation is more intense at higher altitudes (Gates 1962). The study area in
Yellowstone where our experiments were
done is at an altitude of 2,231 m, the
water level over the algal mats is only 1-2
cm thick, and the water itself shows no
absorption in the ultraviolet down to 300
nm. Since the glass vials used in the photosynthesis experiments show strong end
absorption below 350 nm, it was important
to know whether the experiments on the
effect of light intensity were biased owing
to the screening of natural ultraviolet radiation by the glass vials. Inhibition
of
photosynthesis by natural ultraviolet radiation has been reported by Findenegg
(1966) and Rodhe, Hobbie, and Wright
( 1966). Photosynthesis of algal cores was
measured by the 14C method using quartz
336
THOMAS
D. BROCK
TABLE 1. Radioactivity
oj Synechococcus
at different
levels through an algal core”
determined
by autoradiography
Layer
Surface
Next to surface
Next to bottom
Bottom
AND
cetls
as
Labe$d) cells
0
No. silver grains
per labeled cell
95
57
20
35
4.8
3.5
1.8
1.3
* Thickness of core, about 5 mm; each layer analyzed,
about 1.2-1.3
mm. Core 0.75-cm diameter.
Source of
core, station VI, 57C. Incubation
4 hr at temperature of
origin in 1 &i/ml
NaIIrdCO, in 5-ml volume.
Slides for
autoradiography
washed five times in deionized
water,
dipped in Kodak NTB-2 liquid emulsion diluted l/2.5,
exposed four days and processed in Kodak DlB developer.
cuvettes. To ensure the same geo,metry
throughout,
controls, cons,isted of quartz
cuvettes in which all radiation below 350
nm was excluded by the use of four layers
of Saran Wrap (Dow Chemical Co.), a
material showing strong end absorption
below this wavelength,
The average rates
of photosynthesis from two separate experiments were as follows: uncovered quartz
cuvettes, 1,309 cpm hr-1 rug chlorophyll-l;
Saran-covered quartz cuvettes, 1,262 cpm
hr-l lug chlorophyll-l.
Since these results
are not significantly different we conclude
that natural ultraviolet
radiation neither
inhibits nor stimulates photosynthesis, and
that the use of glass vials which do not
pass ultraviolet radiation is therefore justified for light intensity experiments.
Vertical
xonation of photosynthetic
ability in algal cores
The microbial mats in these alkaline hot
spring channels consist of a compact thin
layer of algae enmeshed in a matrix of
filamentous bacteria on top of a thicker
layer of bacteria alone. The thickness of
the upper layer containing algae is usually
about 0.5 cm and the thickness of the
whole core varies from 1 to 2 cm. Since
the algae require light for growth, it
seemed likely that the thickness of the
algal layer is determined by self-shading.
To verify this, the photosynthetic
ability of
algae at different levels through the 0.5cm
algal layer was determined by quantitative
autoradiography.
Cores were incubated in
M.
LOUISE
B-ROCK
high concentrations of NaII14COs (1 &i/
ml) for 4 hr to ensure heavy labeling, and
layers about 1.5 mm thick were removed
and macerated; the resulting suspensions
were used to prepare slides for autoradiography ( Brock and Brock I968u).
After
exposure and processing, the radioactivity
of the cells was determined by counting
the number of silver grains per SynechoCOCCUS cell (Table
1). Photosynthesis is
maximal in the surface layer and falls off
progressively in the deeper portions of the
core, but some photosynthesis still occurs
in the lower portions of the core. These
results, which confirm the hypo,thesis of
self-shading, are of considerable significance in interpreting
the results of the
later experiments on the effect of light
intensity on photosynthesis.
The autoradiographic
studies reported in Table 1
were done with algae from a temperature
of 57C, where algal standing crop is the
highest (Brock and Brock 1966; Brock
1967a). At higher temperatures, the thin
cores made it impossible to perform similar
studies. It seems unlikely, however, that
self-shading occurs, in the thin mats at
these higher temperatures.
Effect of light intensity on photosynthesis by normul algal populations
Experiments have been done to measure
the rate of photosynthesis of the algal populations at different light intensities. Light
intensity was reduced using neutral density
filters. Most of the experiments were done
on clear, cloudless days when insolation
was maximal, in the summers of 1966,
1967, and 1968, and in February 1968, at
various stations along the thermal gradient from a temperature of 7OC down to
55C. Representative results are given in
Tables 2 and 3. In general there is little
evidence of light inhibition at full sunlight,
and the rate of photosynthesis falls as light
decreases. From these data the rate of
photosynthesis per unit of sunlight was
calculated, so that the efficiency of light
utilization could be determined (Tables 2
and 3). The efficiency of utilization
of
sunlight is usually greatest at intensities
PIIOTOSYNTIIESIS
TABLE 2.
Filter
% transmission
100
70
44
14
7
0
Effect
BY
of light intensity
W
0.55
0.39
0.24
0.08
0.04
0
* Light intensity
t Photosynthesis
1,700
1,300
870
170
26
26
P/L1
100
70
4
14
7
0
at station
I, 71C
Expt 3 (13 July 1967)
3,200
3,500
3,600
2,200
680
-
P
P/L1
LI
1.3
0.92
0.56
0.18
0.09
0
1,100
1,500
1,100
390
300
26
870
1,600
1,900
2,200
3,300
-
1.2
0.86
0.54
0.18
0.09
0
P
P/L1
1,800
2,100
1,500
420
46
74
1,500
2,400
2,700
2,400
520
-
expressed as g cal cm-2 min-?
expressed as cpm hr-1 ,ug chlorophyll-‘.
Adaptation to reduced light
The fact that there was little or no
inhibition
of photosynthesis by high light
intensities suggested that perhaps the algae
were completely
adapted to high light
conditions,
Therefore, we experimentally
reduced the light over portions of the algal
mats and determined the response to light
intensity after various times 0.f adaptation.
A gray glass was used to reduce the light
intensity
(“Gray
Lite”
#52, Pittsburgh
Plate Glass Co. ) . The absorption spectrum
of this glass is not precisely neutral, as it
shows minor absorption peaks at 650, 590,
and 540 nm as well as troughs at 560 and
400 nm; we assumed that these minor diversions were not significant for this work.
When two layers of this glass each 1/ inch
( 0.64 cm) thick were placed together, the
light intensity was reduced 82%, and this
combination
was used in the following
work. The plates of glass ( 46 x 61 cm)
Filter
5%transmission
on photosynthesis
LI
7-14% of full sunlight, although photosynthesis is actually less than at high light
intensities.
TABLE 3.
337
ALGAE
Expt 2 (10 July 1967)
Expt 1 (6 July 1967)
LI*
TIIERMAL
Effect
of light intensity
on photosynthesis
at various
(For units, see Table 2)
Station II (68C)
LI
1.3
0.89
0.56
0.18
0.09
0
P
1,200
1,400
1,200
850
340
50
were suspcndcd by a wooden framework
just above the water surface (see Fig. 3,
Brock and Brock 1968Ir). Glass was installed on 2 August 1967 over areas of
algal mat immediately below stations I, II,
III!& and VI. Station 111% had to be
abandoned later when the channel in this
region was altered by a hailstorm, but the
glass at the other stations has been maintained in place for over a year.
Within two days after the glass plates
were installed, the algal mats under them
became noticeably darker green than the
control areas, and they became progressively darker over the next two weeks.
Table 4 shows that the visual observations
of rapid increase in chlorophyll
content
were not confirmed by the quantitative
assays. The most reasonable explanation
is that the changes seen occurred only in
the algal populations
at the immediate
surface of the mat, whereas the quantitative measurements reflect the chlorophyll
content of the whole core.
In Table 5, comparisons are made between equivalent stations, one in full sun-
hot spring
stations,
Station 111% (65C)
P/L1
940
1,600
2,200
4,800
3,800
-
13 July 1967.
Station VI (58C)
LI
P
P/L1
LI
P
P/L1
1.2
0.84
0.53
0.17
0.08
0
1,200
800
850
400
250
82
1,000
950
1,600
2,400
2,900
-
1.2
0.82
0.51
0.17
0.08
0
880
840
820
510
300
63
760
1,000
1,600
3,100
3,600
-
338
THOMAS
TABLE 4. Changes
after installation
0*
3
in chlorophyll
and cell count
neutral density glass at
station II
7.4
7.3
8.7
8.9
9.3
8.0
6.3
21
12
z
13
50
186 (winter)
299
333
* 2 August
AND
of
Chl a
(fig/core)
Day
D. BROCK
No. cells/
core
Chl (bg/
10’ cells)
Tcmp
(“C)
10 x 10’
8.6 x 10’
15 x 10’
3.5 x 10’
12 x 10’
-
0.74
0.85
0.56
1.8
1.9
-
68.5
66.4
70.0
69.5
71.5
69.5
66.5
66.5
66.5
1967.
light and another which had been under
glass for 299 days. In all cases the cell
counts of the stations in reduced light are
lower than those in full sunlight. To adjust
for these differences, chlorophyll values are
also reported as the amount of chlorophyll
per cell. At stations I and II the populations under reduced light have more chlorophyll per cell than those in full light,
whereas at station VI the two populations
have essentially the same values. Presumably at station VI the algal mat is
sufficiently
thick so that self-shading is
complete in full sunlight, whereas at stations I and II the thinner algal mats result
in incomplete self-shading, permitting the
entire algal mat to adapt to reduced light.
Since even at station VI the mat under the
glass was noticeably greener than that of
the control station, we assume that adaptation to reduced light by the surface algal
material has occurred here, although we
h ave no way of detecting
it by our
measurements. In Table 5 one set of meaTABLE 5.
Comparison
of chlorophyll
M.
BROCK
surements is given for station II in winter, when more frequent cloudy days and
shorter day length results in reduced light
intensity and less total light. There is an
increase in chlorophyll content per cell in
the control winter samples compared to
summer samples, except at station VI. All
of the algal mats of the alkaline hot springs
are markedly darker green in winter than
in summer, although these differences also
are not revealed dramatically by quantitative determinations except at temperatures
near the upper limit for algal growth,
where because of the very thin mats, selfshading is minimal.
Effect of light intensity on photosynthesis
by populations adapted to reduced light
Tables 6 and 7 present data on the
effects of light intensity on photosynthesis
of algal populations at stations II and VI
adapted for varying periods of time to
reduced light. Although the general picture is similar to that of Tables 2 and 3,
two differences should be noted. The expected inhibition of photosynthesis by full
sunlight is noted occasionally in the populations adapted to reduced light. For station II (Table 6) the efficiency of photosynthesis at the low light intensity, 7% of
full sunlight, is less than that of the unadapted populaton
( Table 3)) which is
surprising, as it might have been anticipated that the populations adapted to low
light would be able to use it more efficiently. The increased chlorophyll content
of the surface layers might result in increased shading of the lower layers,
thereby diminishing the ability of the core
as a whole to use low light intensities.
and cell count of stations
reduced sunlight (R)
Chl a (fig/core)
Days
Station
LOUISE
in full
sunlight
(F)
and those in
Chl/ 10’ cells
No. cells/core
F
R
F
R
F
R
8.6
13
57
17
21
27
11 x 10’
13 x lo7
29 x loq
7.0 x lo7
12, x lo7
14 x lo7
0.81
0.99
1.9
2.4
1.8
1.9
9.9 x 10’
3.5 x lo7
1.3
1.8
299
I
II
VI
186
II
(winter)
13,
6.3
PHOTOSYNTHESIS
TABLE
BY
THERMAL
339
ALGAE
of algal populations at station II adapted for dif6. Effect of light intensity on photosynthesis
ferent periods of tim.e to reduced light. (1870 of full sunlight; for units, see Table 2; day 0,
2 August 1967)
Filter
% transmission
100
70
44
14
7
0
333 days
186 days
13 days
LI
P
P/L1
LI
P
P/L1
LI
P
P/L1
1.4
0.99
0.63
0.20
0.10
0
360
550
650
620
31
6
260
560
1,000
3,100
310
-
1.1
0.79
0.50
0.16
0.08
0
500
410
390
320
13
12
450
520
780
2,000
160
-
1.2
0.86
0.54
0.17
0.09
0
530
940
830
620
55
40
440
1,100
1,500
3,600
610
-
This reduced efficiency in the use of low
is not noted for the
light intensities
adapted population at station VI.
DISCUSSION
The response to light of a compact algal
mat such as is found in thermal springs is
much more complex than that of algal
suspensions, either in nature or in laboratory cultures. Perhaps the most surprising
aspect of our results is how slowly and
imperfectly
the hot spring algal populations adapt to a changing light regime.
The reasons for this seem obvious, howresults
ever, from the autoradiographic
which show that even within an algal mat
0.5 cm thick the rate of photosynthesis was
markedly reduced in the lower portions of
the core, probably due to self-shading. Although visual observations show that the
thin surface layer of the algal mat rapidly
adapts to reduced light, the mat as a whole
adapts slowly. Unfortunately,
it has not
been possible to devise simple methods for
analyzing responses to light of the algae at
different levels within the mat because of
the difficulty
of separating various strata
of cells accurately.
The absence of a striking inhibition
of
photosynthesis by full sunlight in the natural mats is noteworthy. Light inhibition has
been frequently reported in aquatic algal
populations (reviewed by Goldman et al.
1963) and the concept of sun and shade
phytoplankton
was discussed by Yentsch
and Lee ( 1966). Recently Brown and
Richardson (1968) have described the responses of a variety of algal cultures to
varying light intensities and have shown
that the blue-green algae in general are
sensitive to high light intensities. The light
intensities which the hot spring algae arc
exposed to in Yellowstone are considerably
higher than those experienced by most
other algae. At the altitude of Yellowstone,
2,133-2,148 m, light intensities are considerably higher than at sea level, and clear
skies often prevail for many days or weeks.
Further, the water over the algal mats is
usually shallow, so that little of the available light is absorbed by the water. Thus
it might have been anticipated that full
sunlight would inhibit photosynthesis. That
it does not is probably a reflection of the
compact nature of the algal mat which
ensures extensive self-shading. Only after
reduced light intensities had been maintained over the algal mats for many weeks
did light inhibition by full sunlight become
evident. The absence of an effect of natural ultraviolet radiation on algal photosynthesis is probably also due to self-shading.
TABLE
7. Effect of light intensity
on photosynthesis of algal populations
at station VI adapted
for different periods of time to reduced light.
(180/o of full sunlight; for units, set Table 2; day 0,
2 August 1967)
Filter
70 transmission
LI
P
P/L1
LI
100
70
44
14
7
0
1.4
1.0
0.64
0.20
0.10
0
1,400
1,200
1,100
870
560
47-
1,000
1,200
1,700
4,400
5,600
1.3
0.93
0.59
0.19
0.09
0
13 days
333 days
P
P/L1
710
550
1,200 1,300
1,000 1,700
740 3,900
220 2,400
58
-
340
THOMAS
D. BROCK
AND
Electron microscopic evidence of adaptation of the algae to reduced light has
been obtained by the authors in collaboration with Dr. M. Edwards. Algal cells were
removed with a micropipette from the surface layers of mats that had developed
under both full and reduced sunlight. Observations of ultrathin
sections revealed
that cells taken from habitats in full sunlight had few thylakoids (photosynthetic
membranes), whereas cells from habitats
where light had been experimentally
reduced for a year had extensive photosynthe tic membrane systems.
The upper temperature limit for photosynthetic organisms is about 73C (Brock
1967c). It was of interest to know if the
algae found near this upper limit could
maintain populations throughout the year,
despite the considerable variation in total
amount of light available. Observations of
hot spring algae in Yellowstone have shown
that the upper temperature limit is the
same in winter as in summer. Our expcrimental studies using neutral density glass
to reduce available light to 18% of full
sunlight have also shown that the algal
populations maintain themselves in a nearly
steady state throughout the year. Because
insolation does not significantly
affect the
temperature of a hot spring habitat, the
ability of the algal population to maintain
itself at low light intensities is more critical than it would be in other aquatic
environments,
since in the hot springs
respiratory activity is presumably undiminished in the winter.
The situation in Yellowstone can be compared with that of Iceland, which because
of its higher latitude has a greatly reduced
day length in winter. Tuxen (1944) has
calculated that in Iceland a hot spring alga
will receive 50 times more light in June
than in December and has estimated that
for at least two months around the winter
solstice there will not be sufficient light for
photosynthesis to exceed day and night
respiration. According to the direct observations of Schwabe ( 1936), life in Icclandic hot springs comes to an apparent
stop from November to January. Our own
M.
LOUISE
BROCK
observations are in agreement since an Icelandic spring which had high standing
crops when we first sampled it in late July
(Brock and Brock 1966) had low standing
crops in early May of the following year,
and the upper temperature limit was about
15 degrees lower, presumably because the
algal mat had not recovered completely
from the previous winter. We have been
able to duplicate Icelandic conditions in
Yellowstone even in summer by the use of
opaque filters ( Brock and Brock 1968b) ;
the rate of algal disappearance in complete
darkness is rapid, usually being complete
within a month.
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BROCK, M. L., AND T. D. BROCK. 1968~. The
application
of micro-autoradiographic
techniques to ecological
studies.
Mitt. Intern.
Ver. Limnol. No. 15. 29 p.
1967a.
Relationship
between
BRWK,
T. D.
standing crop and primary productivity
along
a hot spring thermal gradient.
Ecology, 48:
566-571.
-.
1967b. Microorganisms
adapted to high
Nature, 214: 882-885.
temperatures.
Life
at high
temperatures.
-*
1967c.
Science, 158 : 1012-1019.
1966. Temperature
-,
AND M. I,. BROCK.
optima for algal development
in Yellowstone
Nature, 209: 733and Iceland hot springs.
734.
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AND --.
1967. The measurement
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photophosphorylation,
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in benthic algal mats. Limnol. Oceanog., 12: 600605.
196%.
The measurement
-,
AND -.
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J. Bacterial.,
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811-815.
BROWN, T. E., AND I?. L. RICHARDSON. 1968.
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J. Phycol., 4: 38-54.
COPELAND, J. J.
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Ann. N.Y. Acad. Sci., 36:
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l-229.
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