July
LIMNOLOGY
1973
VOLUAME
AND
OCEANOGRAPHY
ENVIRONMENTAL
NUMBER
XVILI
4
CONTROL OF PHYTOPLANKTON
CELL SIZE
T. R. Parsons and M. Takahmhi
Institute of Oceanography,
University
of British Columbia, Vancouver
ABSTRACT
The size of phytoplankton species present in the ocean may be in part determined by
environmental and Dhvsioloeical factors as demonstrated with two phytoplankters, DityZum
brightwellii and Cokblithu~ huxleyi.
In the aquatic environment
it has been
that the size of organisms at any
trophic level can be a determinate factor
in the length of the food chain, the ecological efficiency of energy transfer, and the
type of organisms living at the highest
trophic level (Brooks and Dodson 1965;
Ryther 1969; Parsons and LeBrasseur 1970).
These relationships were brought together
by Ryther (1969) to show that the yield
of fish from a marine ecosystem predominated by phytoplankton
with large cells,
such as the Peruvian upwelling, was much
greater than from areas predominated by
phytoplankton with small cells, such as the
subarctic North Pacific. It may also be
speculated, on the basis of these two extreme environments, that within a specific
environment the yield of fish in any one
season could be determined to some extent
by factors favoring the production of species of phytoplankton having large or small
cells; if it is possible to demonstrate the
validity of this approach, a new aspect to
ocean production assessment will be available. This might explain the present inadequacy of relationships between primary
production and fish production, when these
suggested
LIMNOLOGY
AND
OCEANOGRAPHY
are based only on units of biomass produced per year.
Semina (1972) has summarized some
Soviet data on the mean size of phytoplankton cells in the Pacific Ocean and has
suggested some environmental factors that
may govern the production of species having small or large cells. Although
the
publication has a most useful approach we
believe that it also contains certain discrepancies that should be corrected to
improve the general concept of environmental control of phytoplankton
cell size.
In particular Semina refers to the regions
of the Antarctic and Peruvian upwellings
as being predominated by small-cell phytoplankton, while the size of the herbivores
(krill and anchovy) as well as published
data ( Marr 1962; Ryther et al. 1971) indicate that there are many large-celled phytoplankton in these areas. Also Semina considered only three factors as determining
the cell size of the phytoplankton:
the
phosphate concentration of the water, the
density gradient of the main pycnocline,
and the velocity of vertical water movement. We agree that in part these factors
may contribute to phytoplankton
cell size
511
JULY
1973, V. 18(4)
512
T.
R. PARSONS
AND
selectivity but we believe that on the basis
of ecological and physiological
data a
better grouping
of determinate
factors
would bc 1) the rate of nitrate or ammonia
input to the cell, 2) the extinction coefficient of the water, 3) the mixed layer
depth, 4) the light intensity, 5) the sinking
rate of phytoplankton, and 6) the upwelling
velocity of the water. Of these factors, the
rate of nutrient input to a cell may need
some further clarification
in the light of
recent research.
Dugdale (1967) was the first to discuss
the competitive
advantage of different
phytoplankton
growth rates, to the extent
that these could be determined by different
nutrient concentrations.
He assumed that
the uptake of nutrients by individual species was related to the in situ nutrient
concentration in a form defined by the
Michaelis-Menten
expression. Eppley et al.
(1969) and Eppley and Thomas (1969)
provided experimental evidence to show
the close relationship between the specific
growth rate of a phytoplankton
cell and
the in situ concentration of nutrient. More
recently Droop (1970) and Caperon and
Meyer (1972) h ave shown that in shortterm experiments, the instantaneous growth
rate of a phytoplankter
is related to the
nutrient
concentration
within
the cells
rather than the nutrient concentration in
the environment.
Although these results
may be accepted, it is apparent that plankton cells in nature will have become preconditioned to an average concentration of
rate-limiting
nutrient and that this can be
used for the purpose of examining the
specific growth rate of phytoplankton under
field conditions.
Therefore a direct relationship between the in situ nutrient concentration and the specific algal growth
rate appears to be a justified approximation
for the following discussion.
RESULTS
AND
DISCUSSION
The determinate factor in the predominance of one cell size over another will
be the growth rate of the phytoplankton as
described in the equation
nt = n, efit,
(1)
M.
TAKAHASIII
where, n, and nt are the standing
phytoplankton at the beginning of
of observation and at time t, and
growth constant characteristic of
ticular size group of phytoplankton.
1 to 6 above can then be related to
equation
stocks of
a period
p is the
the parFactors
p by the
where, pI,I(,Xis the maximum growth rate of
the species or size group, [N] is the nitrate
concentration, S is the sinking rate, U is
the rate of upwelling, and D is the mixed
1ayer depth. K1 and KN are MichaelisMenten constants characteristic of the nutrient and light response of the species or
size group. < I > is the average photosynthetic light intensity in the water column
as determined by
(I) = (Io/kD)
(l-e-““),
(3)
where I0 is the surface photosynthetic light,
k is the average extinction coefficient, and
D is the depth of the mixed layer.
Sufficient evidence exists (Paasche 1967,
1968; Eppley et al. 1969; Smayda 1970) to
show that there are physiological
differences between large and small phytoplankton cells in the terms KI, &, and S. In
particular we have chosen two species, the
large Ditylum brightwellii
and the small
Coccolithus hale yi, and entered physiological values for these variables in Table I.
Table 1. Physiological properties of cells from
Eppley et al. (1969) and Smayda (1970)
C.
Diameter
(11)
30
huxteyi
5
IJmax
(doublings/day)
2.32
1.75
KI (b/min)
0.009
0.002
Sinking
h/day)
rate
(healk~
cells)
2.0
(senescent cells)
(no coLA.ths)
1.5
coccoliths)
(with
PHYTOPLANKTON
Table 2.
Subarctic Pacific
(spring)
Subtropical
(summer)
Tropical
upwelling
Antarctic
upwelling
(summer)
Coastal estuarine
(spring)
Upwelling
(cm/day)
250
2
500
0
Note:
<I>
(ly/mid
0.080
100
0.011
0.035
100
0.048
20
10
10
0.095
0.095
25
50
0.068
0.029
200
2
10
0.250
3
0.050
these results it is apparent that the growth
rates for C. huxleyi are higher than those
for D. brightzoellii
in areas which are
known to be predominated by small-celled
phytoplankton
(e.g. stable subtropical seas
such as the Sargasso Sea and temperate
waters such as the subarctic Pacific).
On
the other hand the larger phytoplankton
species shows a higher growth rate in areas
of tropical and antarctic upwelling as well
as in coastal environments; this also is in
general agreement with current observations.
brightwellii and Coccolithus huxleyi under different
mental conditions
(doublings/day)
Antarctic
upwelling
(summer)
Coastal estuarine
(wring)
0.5
D
(m>
20
D. brightidlii
Subarctic Pacific
(wring)
Subtropical
(summer)
Tropical upwelling,
20
(m'l)
500
Growth constants of Dityluln
Area
Nitrate
@g-atom/liter)
400
Further,
the environmental
factors described by the terms IO, 7c, D, and U are
sufficiently different for us to give approximate values for different oceanic environments ( Table 2). The values in Tables 1
and 2 could be larger or smaller with other
species and other environments, but the
range of values given is sufficient for the
purposes of our discussion.
By applying values for the species of
phytoplankton
and different environments
to equation 2 we have determined phytoplankton growth rates ( Table 3). From
Table 3.
513
SIZE
Some estimates of environmental properties in different marine areas
Radiation
(b/W)
Area
CELL
C. huxleyi
enuiron-
Comments
(doublings/day)
1.22
1.46
Healthy cells;
no coccoliths
0.84
1.37
1.90
1.59
1.66
1.61
1.48
0.80
Senescent cells;
with coccoliths
Healthy cells;
with coccoliths
Healthy cells;
no coccoliths
Healthy cells;
with coccoliths
The choice between parameters favoring healthy cells or senescent cells
and with or without coccoliths
was made on the basis of nitrate
concentration
and average light intensity,
Table 2,
Cells were assumed to be healthy in
high nitrate
environments and coccoliths
were presumed present in high light
intensity
environments,
514
T.
IL
PARSONS
AND
Fig. 1. Three-dimensional graph showing the
effect of light and nutrients on the ratio of Ditylum
brightwellii growth rates to Coccolithus huxleyi
growth rates. (Values of ,.Aratio > 1 indicate a
predominance of D. brightwellii over C. huxleyi. )
A three-dimensional
graph has been
drawn showing changes in the growth rate
ratio, D. brightwellii: C. huxlqi
( Fig. 1).
For the purposes of this graph, the term
(S - U) / D in equation 2 was set equal to
zero and only the variables p, < I >, and
N were considered. The graph illustrates
that only in a region of high light intensity
and high nutrient concentration is it possible for the large phytoplankter
to grow
faster than the small phytoplankter.
This
may help to explain two rather general
observations made by aquatic ecologists.
The first is that the nannoplankton ( < 20-p
diam) have often been observed to be the
principal autotrophic organisms in marine
environments; except in taxonomic studies,
the larger net phytoplankton
are seldom
considered to be representative of the total
primary production in many areas. The
second observation is that conditions of
eutrophication
in lakes are generally accompanied by reports of an increase in net
phytoplankton associated with the eutrophication process. Since maximum phytoplankton growth under eutrophic conditions also occurs mostly during summer, it
is evident that there is some ecological
support for the high light, high nutrient
region of large-cell production indicated in
Fig. 1. Another possible application of the
general concept suggested by Fig. 1 is that
it may account for the seasonal succession
M.
TAKAHASHI
in the cell size of coastal phytoplankton.
In this respect Loftus et al. (1972) found
a general relationship between the cell size
of phytoplankton in an estuary, before and
after a pulse of rainfaI1, and the KN values
for different sized species as suggested by
Eppley et al. ( 1969).
If the term ( S-U) / D is included in additional three-dimensional graphs it is further
apparent that the zone of large phytoplankton cell production in Fig. 1 can be extended or retracted depending
on the
ability of large-cell species to decrease their
sinking rate ( Smayda 1970). Also a high
rate of upwelling,
especially in shallow
mixed water columns such as may occur in
estuaries and some lakes, will tend to favor
large-cell production.
The arguments presented in this discussion have depended on data on only two
species, of different cell size, chosen because sufficient data were available about
them to use equation 2. It is quite apparent,
however, from additional data accumulated
by Eppley et a1. ( 1969)) Eppley ( 1970))
and Smayda (1970), that the range of
physiological constants ( K1, KN, and S) for
other species of different cell size would
generally support the conclusions reached
from Table 3 and Fig. 1.
Three factors that might be added to
equation 2 are the compensation light intensity, temperature coefficients, and the
relative size selectivity of zooplankton grazing. We do not at present have any data
on the compensation light intensities of the
two species discussed here, but obviously
differences in respiration, which would be
covered by this term, must exist between
the two species. Similarly we do not have
specific information
on their temperature
coefficients, although Eppley ( 1972) has
shown that this is an important parameter
in determining
photosynthetic
rate. The
effect of size selective grazing has been
discussed by Malone ( 1971)) who showed
that the final standing stock of net plankton
and nannoplankton in tropical oceanic and
neritic communities could be governed in
part by size selectivity by grazing ZOOplankton.
PIlYTOPLANKTON
REFERENCES
J. L., ANU S. I. DODSON.
1965. Predation, body size, and composition of plankton.
Science 150: 28-35.
CAPERON,
J., AND J. MEYER.
1972. Nitrogen
limited growth of marine phytoplankton-l.
Deep-Sea Res. 19: 601-618.
DROOP,
M. R. 1970. Vitamin Bla and marine
ecology 5. Helgol. Wiss. Mceresunters. 20:
BROOKS,
629-636.
R. C. 1967. Nutrient limitation. in
the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12 : 685-695.
EPPLEY,
R. W. 1970. Relationships of phytoplankton species distribution to the depth
distribution of nitrate. Bull. Scripps Inst.
Oceanogr. 17 : 43-49.
1972. Temperature
and phytoplank-.
ton growth in the sea. Fish. Bull. 70: 10631085.
1969.
-,
J. N. ROGEHS,AND J. J, MCCARTHY.
Half saturation constants for uptake of nitrate
an d ammonium by marine phytoplankton.
Limnol. Oceanogr. 14: 912-920.
1969. CompariAND W. I-1. THOMAS.
son of half-saturation “constants” for growth
and nitrate uptake of marine phytoplankton.
J. Phycol. 5: 365-369.
LOFTUS,
M. E., D. V. SUIJISA RAO, AND I-1. I-1.
SELIGER.
1972. Growth and dissipation of
phytoplankton in Chesapeake Bay. 1. Chesapeake Sci. 13: 282-299.
MALONE,
T. C. 1971. The relative importance
of nannoplankton and netplankton as primary
producers in tropical and neritic phytoplank-
DUGUALE,
CELL
SIZE
515
ton communities. Limnol. Oceanogr. 16 :
633-639.
MAI~R, J. W. S. 1962. The natural history and
geography of the Antarctic krill (Euphausia
superba Dana). Discovery Rep. 32: 33464.
1967. Marine plankton algae grown
PAASCI-IE, E.
with light-dark cycles. 1. Coccolithus huxZeyii. Physiol. Plant. 20: 946-956.
-.
1968. Marine plankton algae grown
with light-dark cycles. 2. Ditylum brightwe&i
and Nitzschia
turgidula.
Physiol.
Plant. 21: 66-77.
PARSONS, T. R., AND R. J. LEBRASSEUR.
1970.
The availability of food to different trophic
levels in the marine food chain, p. 325-343.
In J. I-1. Steele [ed.] Marine food chains.
Oliver and Boyd.
RYTI-mn, J, H. 1969. Photosynthesis and fish
production in the sea. The production of
organic matter and its conversion to higher
forms of life vary throughout the world
ocean. Science 166: 72-76.
D. W. MENZEL, II. M. HULBERT,
C. J,
L&ENZEN,
AND N. CORWIN.
1971. The
production and utilization of organic matter
in the Peru coastal current. Invest. Pcsq.
35: 43-59.
SEMINA,
I-1. J. 1972. The size of phytoplankton
cells in the Pacific Ocean. Int. Rev. Gesamten Hydrobiol. 57: 177-205.
SMAYDA,
T. J. 1970. The suspension and sinking of phytoplankton in the sea. Oceanogr.
Mar. Biol. Annu. Rev. 8: 353-414.
Submittecl: 4 January 1973
Accepted: 4 April 1973