Limnol. Oceanogr., 36(8), 1991, 1886-1898
0 199 1, by the American
Society
of Limnology
and Oceanography,
Inc.
Rates of phytoplankton cell division in the fib
iron enrichment experiments
Karl Banse
School of Oceanography WB-10, University of Washington, Seattle 98 195
Abstract
Increases in chlorophyll with time for contained coastal plankton, expressed as daily division
rates, are on average about as high as rates for nutrient-replete cultures at similar temperatures,
when daylength is considered. In offshore areas with persistent high nutrients but low chlorophyll,
division rates from increased chlorophyll and cumulative NO, uptake in the controls of Fe enrichments are on average also high and do not suggestmarked Fe deficiency. The normally observed
phytoplankton growth in the controls is interpreted as due to release from grazing. Addition of Fe
in the treatments leads to blooms and exhaustion of NO,. Differences between controls and treatments in rates of chlorophyll increase and NO, removal, however, as well as shifts in species
composition toward rare species in the treatments, also indicate direct effects of Fe on phytoplankton. To clarify the issues, especially in respect to medium- and large-celled phytoplankton, I
recommend measurements of species-specific division rates.
In the large offshore areas of the subarctic
Pacihc, the eastern equatorial Pacific, and
the subantarctic,
circumpolar
Southern
Ocean, concentrations of macronutrients (N,
P, Si) are always high, but those of chlorophyll are low even in summer; for the
most part, phytoplankton
biomass resides
in, and most of the primary production rate
rests on, small cells (Cullen 199 1; Frost
199 1). The primary production rate is the
product of phytoplankton concentration and
the specific growth rate averaged over the
community, and the specific growth rate is
proportional to the rate of cell division. The
phytoplankton concentration is maintained
by a balance between the rates of gain and
loss of cells. To help in understanding the
processes underlying such a balance in the
sea, my paper compares newly derived cell
division rates in control bottles of shipboard enrichment experiments, planned to
show limitation
of phytoplankton
growth
from Fe deficiency, with published values
from coastal waters where Fe limitation
of
Acknowledgments
My attendance at the symposium was fully supported and the preparation of the manuscript partially
supported by NASA (Oceanic Productivity Program)
grant NAGW- 1007.
J. R. Postel helped with the computations. The suggestions by two reviewers and D. P. Henry regarding
the content and form are also gratefully acknowledged.
Contribution 1916 from the School of Oceanography, llniversity of Washington.
division rates presumably did not prevail.
The measurements are normalized by temperature. This variable is chosen because it
appears to be the principal environmental
difference for phytoplankton from nutrientrich subpolar and equatorial seas; at least
in summer, daylength at the higher latitudes
largely compensates for the greater hourly
incident irradiance of the lower latitudes. I
do not address the maintenance of the biomass level presently found or the change in
biomass and, hence, production rate, which
may result from an eventual field manipulation.
In the absence of animals, healthy phytoplankton illuminated in a bottle with replete nutrients will grow exponentially
following
X = &expW
(1)
w‘here X, and X0 are the concentrations at
times t and zero and p is the insta.ntaneous
growth coefficient (time-l; unit of d-l here).
The underlying dX/dt is called herein the
population growth rate when referring to
single species and the bulk population
growth rate when the increase of the phytoplankton as a whole is considered in the
absence of grazing or other losses; the latter
term is applied also to natural plankton when
the effect of grazing is experimentally
excluded, as in dilution or chlorophyll-labeling techniques. As long as nutrients do not
terminate population growth, X, is time-de-
1886
Phytoplankton division rates
pendent, while p over a wide range of nutrient concentrations is not, so that p is the
preferred criterion of physiological condition.
With zooplankton present in the bottle,
as in the natural water used in the published
Fe enrichment assays, Eq. 1 becomes
X = &expK~ - m>tl
where m is the instantaneous death rate of
the phytoplankton
from grazing and enclosure effects. The underlying dX/dt is called
herein the net population growth rate when
referring to individual species and the phytoplankton community
growth rate when
addressing the phytoplankton as a whole (e.g.
as chlorophyll).
The difference (p - m) is
the instantaneous net community
growth
coefficient. In the seas of concern, the nearabsence of time dependence of X, (the accumulated biomass) indicates again the utility of studying p instead of terminal yield
of cells or chlorophyll,
as these might be
measured in an enrichment experiment.
It can be shown for the seas of concern
that the physically caused losses of phytoplankton (from vertical advection, diffusion, and sinking) are small relative to division rates during most of the year, so that
the principal process determining m must
be grazing (Frost 199 1). Grazing is size-dependent, small (large) animals generally being unable to graze efficiently on large (small)
plant cells, if at all (however, see Longhurst
199 1). Considering further that algal division rates are mildly size-dependent (see below), Eq. 2 can be expressed as
sum
xi(l)
= sum
X&eXp[(fli
-
T?Zi)t].
(3)
In other words, the difference (b - m) in a
mixed community cannot be profitably replaced by a variable r. Instead, it must be
kept in mind that studying enrichment experiments in natural plankton means tackling one equation (Eq. 2) with two unknowns.
In the following sections, maximal instantaneous rates of population growth [d-l,
expressed as division (doubling) rates per
day, div. d-l, from b/in 2 = p/0.693], as
obtained in unialgal or pure cultures under
saturating light with a full complement of
nutrients, will be reviewed as dependent on
1887
temperature, daylength, cell size, taxonomic affiliation, and nutrients, including Fe.
Interactions among these factors, however,
are not considered. The results are compared with newly reviewed community and
bulk population growth rates from coastal
waters, which presumably are not Fe deficient, and with the division rates in the controls of bioassays from offshore waters where
dissolved Fe is presumed to be in short supply. The community growth rates are expressed as community division rates (d-l)
by dividing the instantaneous net community growth coefficients (h - d) by 0.693.
The net population division rate is the homolog for individual species, and it and the
bulk population division rate are obtained
like the community division rate.
Division rates in cultures
This section treats published laboratory
data on division rates of individual
phytoplankton species.
Temperature - Algal division rates in
batch cultures, replete with light (mostly
continuous), COZ, and nutrients, were plotted on temperature by Eppley (1972). The
maximal values fell under an envelope that
described an exponential dependence such
that division rates almost doubled (1.88
times) upon an increase of temperature of
10°C. Numerous data points lay well below
the envelope; Eppley showed that for some
species these values reflected less than optimal temperatures but surmised that for
most the cause could have been differences
in cell size and concentrations of chlorophyll in the cells. The role of the last two
variables for diatoms was treated theoretically by Geider et al. (1986; note that their
figure 3 appears to present division rates),
but only cell size is treated below.
Earlier studies of division rates related to
temperature among phytoplankton
(some
tending to slightly higher dependence, as
mentioned by Eppley 1972; cf. Goldman
and Carpenter 1974 for continuous
cultures) were short on data for near-freezing
temperatures. Also, the functional form of
the dependence has been argued (e.g. Ahlgren 1987). New measurements for lightsaturated Antarctic diatoms (Fig. 1) indicate
that Eppley’s temperature coefficient is rea-
1888
Banse
I
v
I
u
>;
.0
I
I
I
I
I
I
I
1.5-
l.O- *0
A=?
Y0
:
TT
0.5- -4 --,/A-*
a
-AA
I I I
-2
0
co. 12 20
I
2
I
I
4
I
-
I
6
“C
h
Fig. 1. Division rates of algal species in cultures as
dependent on temperature with the “standard curve”
for optimal growth (Eppley 1972) and half of this maximum (broken curve) added. Filled symbols-24 h of
light; other estimated daylengths (h) shown below temperature scale. Double data points indicated by “2.”
From left to right: O-diatoms (Rivkin and Putt 1987);
ranges (bars) and medians (diamonds) for 10 diatoms
(avg max rates, mostly for 24-h days, Gilstad and Sakshaug 1990) for 13 diatoms and 2 others (with clear
size dependence within set, Sommer 1989); A-diatoms (Jacques 1983); O-diatoms (Fiala and Oriol 1990;
note that p instead of division rates had been calculated).
sonably accurate. These data are supported
by observations on net population division
rates in containers of natural Antarctic waters: Spies (1987) studied five diatom species in coastal samples; under continuous
light at - 1°C 27 rates ranged from 0.38 to
1.33 div. d-l (median, 0.70). Buma et al.
(199 1) investigated nine diatom species in
offshore waters; during 16-h days at (terminally) 3. S”C, 13 rates ranged from 0.36
to 0.98 div. d-’ (median, 0.63).
Daylength -Among
papers treating the
effect of daylength on division rates are the
comprehensive
treatments by Brand and
Guillard ( 198 1) and Langdon ( 198 8) and a
study on Arctic diatoms by Gilstad and Sakshaug (1990). No taxonomic pattern is obvious among the responses, which range
from insensitivity
of division rates to daylength to rates at a combination of, for example, 10 h x - 50 pmol mm2 s-l being
higher than at 4 h of saturating irradiances
of 500 pmol mm2 s-’ (division rates may
differ more than twofold; example from Gilstad and Sakshaug) and to inability to grow
under continuous light. Thus, the average
division rate of mixed phytoplankton under
replete light and nutrients might not come
close to the value expected from temperature alone.
cell size (mass)-In contrast to most other organisms, the dependence of division
rates on cell size is mild among phytoplankton-the
maximal (optimal) rates in diatoms and dinoflagellates at 20°C approximately being halved upon a lOO-fold to
200-fold increase in cell C (from linear predictive regression) or upon an increase of
-30-fold
[from model-2 regression (divide
the former mass dependence by the correlation coefficient); both ranges calculated
from Banse 19821. The mild mass dependence was confirmed by Sommer (1989) for
diatoms at 0°C. Even so, large-celled phytoplankton species, growing under saturating light with replete nutrients, cannot come
close to the division rates expected from
temperature alone, and mixed diatom assemblages also may not be able to do so.
Note: Schlesinger et al. (198 1) and Langdon
(1988) in equations that lumped large taxa, calculated steeper exponents of dependence of growth
(division) rates on cell C than reported by, for
example, Banse (1982) and Sommer (1989) for
diatoms or dinoflagellates. Clearly in Schlesinger’s data set (their figure 1), the relation was unduly weighted (steepened) by the inclusion of
many small diatoms and several large non-diatoms. Because of the differences in maximal division rates among major algal taxa (see below),
a re-evaluation of the equations of Schlesinger et
al. and Langdon is in order.
Taxonomic afiliation -Earlier I showed
(Banse 1982) that, at the same cell volume
(C content) and at 20°C division rates of
medium-sized diatoms are -3 times those
of dinoflagellates of the same size. 1 mentioned that those of 19 species from other
algal groups and the Cyanophyceae fell
largely between diatoms and dinoflagellates,
with a few growing even more slowly than
the average dinoflagellate of the same size.
The field data of Furnas (1982, 1991) and
Landry et al. (1984), as well as the review
by Furnas (1990), support this generalization. Again, the average division rate of
mixed phytoplankton under replete light and
nutrients might not come close to the value
expected from temperature alone.
Phytoplankton division rates
1889
Macronutrients- Because this paper fo- ever, Rich and Morel (1990) stated that, if
growth in the open sea is
cuses on nutrient-rich
seas, little needs to phytoplankton
be said about nutrients vs. division rates. limited by Fe, slow kinetics of Fe solubilization must be the reason.
In view of the suggested Fe fertilization project in the Southern Ocean (Martin et al.
1990a), however, two points will be noted. Division rates in the field
This section treats experiments in coastal
First, Zentara and Kamykowski
( 1977)
found that Si04, rather than N03, is apt to waters where I assume Fe is not limiting.
Methods-Division
rates were calculated,
be the limiting nutrient at intermediate and
when incubation temperatures were availhigher latitudes of the western South Pacific.
was
Similarly, low values of SiO, and Si04 : NO3 able and limitation by macronutrients
unlikely, from observed concentrations or
ratios were reported offshore from the Indian sector of the Southern Ocean (Jacques independent evidence (as by Laws et al.
and Minas 198 l), and SiO, exhaustion was 1984). Division rates were found either from
growth rates (chlorophyll
infound to set-in offshore before that of NO3 community
in bioassays in the Scotia-Weddell
Seas creases, simple symbols in Fig. 2; usually,
samples were strained through coarse net(Atlantic sector; Buma et al. 1991). In contrast, near the coast of Antarctica,
Spies ting to remove large zooplankton before incubations) or bulk population growth rates
(1987) observed that PO, was exhausted first
(grazing experimentally
excluded; circled
in two of five large incubation experiments.
symbols in Fig. 2). Average relations for the
Second, Jacques (1983) and, more fully,
Sommer (1986) showed for Antarctic pe- two types of rates were calculated by linear
regression analysis from Eppley’s ( 1972)
lagic diatoms that half-saturation
constants
model,
for SiO,-controlled
growth may be so high
(ranging between 6 and 89 IAM, median 22,
log div. (d-l) = a + b x T(“C).
for five spp.) that some species exhibit greatly reduced growth rates under common,
Plots of the residuals on daylength showed
“nutrient-rich”
conditions.
Sommer and no trend for community and a nonsignifiStabel(1986) reported from the same cruise
cant trend (increase with time) for populaas Sommer (1986) that the observed horition division rates. Also, linear regressions
zontal distribution
relative to the ambient
of log division rate on hours were nonsigSi04 : NO3 ratios of three dominant diatoms
nificant for either group (r2 = 0.003 and
and “other, non-silicious algae” (principal0.0 1, respectively). Therefore, time was nely, cryptophycean flagellates) reflected these glected and the new average relations of diphysiological
properties. In the last-menvisions are dependent on only temperature
tioned data set, then, division rates (and
in Fig. 2. I believe, however, that daylength
hence competition for nutrients) overrode
(incubation period) should play a role and
sinking and grazing losses in determining
that its generally small range in the present
community composition. Thus, the effect of material (Fig. 2), combined with other
macronutrients
on cell division cannot be sources of variability, obscures the effect of
neglected even in the nutrient-rich Southern
time. To prevent premature generalization
Ocean.
of weak equations, I chose not to report the
Micronutrients (Fe) - Fe uptake and Fe- relations (regressions) numerically.
limited growth by marine phytoplankton
Note: Figure 2 does not incorporate division rates
were studied by, among others, Brand et al.
that were estimated by dividing 14C uptake by
(1983), Sunda et al. (199 l), and Morel et al.
initial Chl concentration and multiplying with a
(199 1). Because Michaelis-Menten
kinetics
Chl: C ratio nor cell C calculated from microreign and growth even for oceanic species
scopical counts. Both approaches eliminate the
may be reduced severely or become nil at
effect of grazing to the extent that the 14Cmeasurement is not affected by it (but see Laws 1984),
oceanic concentrations of dissolved Fe, the
but they are afflicted by other error sources. For
element might exert a very large effect on
high growth rates especially, the appropriate didivision rates. Noting the prevailing, relavisor is not initial Chl but mean Chl over the
tively high concentrations of total Fe, howincubation period; further, accurate Chl : C ratios
1890
Banse
3
6
12-13
12-15
8
10 12 14 16
109 91312 1616
v8
18 20
q
22 24 26 28°C
14
121212 h
14
Fig. 2. Division rates for natural marine plankton in enclosures as dependent on temperature, with the
“standard curve” for optimal growth (Eppley 1972) and half of this maximum (broken curve) added. Estimated
daylength (h) shown below temperature scale. Filled symbols- two stations. Dashed line (from regression, see
text) and circled or enclosed symbols-bulk population division rates [results without grazing, from dilution
method, or Chl labeling (the latter for Welschmeyer and Lorenzen 1984; Downs and Lorenzen 1985; Laws et
al. 1984)]; thin line and other symbols- community division rates (from Chl increases). From left: x -Spies
1987; A, A-Paranjape 1987 (samples with excess NO,); O-Taylor and Haberstroh 1988; V-Sakshaug and
Holm-Hansen 1986 (highest values at intermediate n-radiances); + - Kuiper et al. 1983 (examples of high rates,
No. 24, 25; temperature from Jahnke et al. 1983); Cl-Gifford 1988; x -Welschmeyer and Lorenzen 1984 [table
3; @-highest values except for March (second highest); x -means of two highest values for each date; temperatures from original log books]; V-Downs and Lorenzen 1985 [table 3; means of two highest values for
November, January and April, when NO3 and incident irradiance were high (from original log books)]; OWilkerson and Dugdale 1987 (No. 58B 2); V-Riemann
et al. 1988 (enclosure C, 12-19 September); AMcAllister et al. 196 1 (days 4-14) Antia et al. 1963 (days 8-l 5) both at low irradiance; A-Eppley et al. 197 1
(from figure 2, 1l-l 3 July average of NO, and NH, additions; “20“-25”C”); 0-Landry et al. 1984 (temperature
estimated); + -Cullen et al. 1992 [mean of several stations, under low irradiance (moved from Fig. 3, not used
in regression)]; v, V-Laws et al. 1984 (without offshore station F).
are normally not available. In the microscopical
approach, all cells must have been preserved and
counted, and there is variance in the equations
converting cell volumes to C.
Results-Considering
the effects of daylength, cell size, and taxonomic affiliation
on cell division rates in algal cultures, one
might surmise that the bulk population or
community division rates of natural, mixed
phytoplankton,
which grows with replete
nutrients near light saturation, might not
nearly approach the temperature-set maximal rates. In fact, however, as reviewed by
Furnas (1990) and quantified in Fig. 2, natural assemblages initially enclosed in containers may double fast relative to the maximal rate when considering the shorter
periods of illumination
(Eppley’s 1972 envelope for maximal division rates refers to
continuous light). The field results suggest
that, on the average, only phytoplankton
species well suited to the environmental
controls and the simultaneous, size-dependent grazing pressure tend to dominate natural communities; the other species tend to
lose out because of the relentless loss of cells
to the animals. Further, because several data
points in Figs. l-3 fall above the line for
half of Eppley’s maximal rate, although the
incubation periods were not overly long,
Eppley’s curve may underestimate very high
community
division rates where, for example, assemblages dominated by small diatoms grow under a suitable day-night cy-
1891
Phytoplankton division rates
cle. As to be expected, however, Fig. 2 shows
that the community division rates (i.e. some
grazing present) tend to be lower than the
bulk population rates. The intercepts of the
regression-based curves in Fig. 2 differ significantly on the P = 0.05 level, but the
slopes (curvatures in Fig. 2) do not.
The data in Fig. 2 are supported by other
observations that did not meet all selection
criteria. Of Furnas’ (1982) 29 temperate
coastal assemblages, which were restricted
to cells < 10 pm, two-fifths grew at half the
optimal rate (Eppley’s 1972 curve) or faster,
even though exposed to only 13-15 h of
light (16”-22”C, from Chl change; median
rate, 1.25 div. d-l, but 1.55 div. d-l after
omission of four dates without appreciable
growth). Bienfang and Takahashi (1983) reported 1.3,2.2, and 2.5 div. d-l for the <3pm fraction in subtropical coastal seawater
(25”C, 11 h of light; from Chl change). These
two data sets suggest that the curvature of
the line for the community division rates in
Fig. 2 is too low. Using the Chl-labeling
technique, Laws et al. (1984) estimated 2.9
div. d-l (27”C, 12 h of light) at a tropical,
oligotrophic, offshore station. Based on the
same technique, Laws et al. (1987) reported
light-saturated
bulk population
rates of
- 1.7kO.4 div. d-l (25”C, 13 h of light) for
several nutrient-depleted
offshore stations;
these data are included here because independent evidence suggested absence of
growth limitation.
Thus, Laws’ rates support the line for bulk population growth rate
in Fig. 2 well.
Overall, it appears that the Eppley (1972)
relation of maximal division rates, derived
from cultures, approximately holds for natural communities once the shorter exposure
time is discounted; in view of the unsatisfactory statistics on time dependence, more
work on the latter is clearly desirable.
Division rates in the published
Fe assays
In this section, recent Antarctic enrichment experiments data are re-evaluated before division rates from reputedly Fe-limited offshore waters are compared with the
coastal observations shown in Fig. 2.
Re-evaluation -Results
from Fe bioassays were published by Martin et al. (1990a)
for the Ross Sea (Pacific Sector of the
Southern Ocean) and de Baar et al. (1990)
for the Scotia and Weddell Seas (Atlantic
Sector). Both papers reported time changes
of Chl and NO3 in control bottles and in
samples with Fe additions under natural illumination in the presence of grazers. The
pigment change results from the balance between the addition and loss (grazing) of cells
and ought to be evaluated by Eq. 2; without
a grazing estimate, however, the instantaneous rate of pigment change must be estimated from Eq. 1. In contrast, the doubling rate of cumulative NO3 removal results
from a specific activity of phytoplankton
times its concentration; the activity is apt
to be constant during exponential growth
when there is no time change of division
rate (straight lines in semilog plots). This
division rate is a measure of the rate of bulk
population growth because N03, once assimilated, is gone (no release by grazing)
while newly formed Chl in the assays is being grazed. The rate is evaluated by Eq. 1
(cf. Banse 199 1). The doubling rate of cumulative NO3 uptake should be faster than
that of Chl increase, which in fact tends to
be the case [Table 1 and table 1 of Banse
199 1 from the Gulf of Alaska; also McAllister et al. 196 1; Spies 1987 (newly read
from their figures)].
The data by Martin et al. (1990a) were
taken from their figure 2 and those by de
Baar et al. (1990) from their tables. For both
sets, the periods of exponential growth were
judged from semilog plots (the criterion being straight lines) and regressions calculated
with the model
P = ln([X,/&]/At
where X, and X0 are Chl concentration or
cumulative NO3 uptake at times t and zero.
For Martin et al. (1990a), I evaluated only
the controls and the treatments with 5 nmol
Fe kg-l, but did not utilize the NO3 data
from Sta. 1 because of an apparently too
high initial (day 0) value, as well as nonlinearity in the semilog plot, when day 1 was
used as the starting date. Material death (i.e.
disappearance of Chl) occurred in all experiments early on, especially at Sta. 2, where
about three-fourths of the initial pigment
vanished in the first 2 d. Finally, extrapolation of the NO, regressions to time zero
1892
Table 1. Division rates (d-l, from instantaneous rates of change) for Chl increase and cumulative NO, uptake
in bioassays. C-controls; T-Fe treatments (5 nmol kg-’ for Martin et al. 1990a, l-10 nM for de Baar et al.
1990); days in parentheses, with bracketed days preceding digit, if referring to C, and following, if referring to
T; means for Sta. 145 and 158; single values for remainder.
-Martin
et al. 1990~
Days
Chl
NQ
(l-9)
CW110)
Chl
NO,
Sta. 1
0.13
Sta. 2
0.24
0.23*
(2-13181)
Chl
NO,
(6[31-13)
(6-l 3)
Chl
NQ
de Baar et al. 1990
c
Sta. 3
0.16
0.27(*)
Sta. 4
(3-l 1)
(3-l 1)
0.25
0.53
T
0.18
(2-7)
(2-6)
WW’I)
WWI)
0.49
0.42*
0.26
0.35*
0.66
0.82
(l-lO[ll])
(2-l 1)
(2-9)
(4-9)
W-8)
Chl
NO,
* Intercept
Days
(0.4-8)
s 1 rmol
kg-’ (PM) (i.e. large NO,
uptake
C
Sta. 145
0.64
0.72
Sta. 158
0.22
0.29*
Sta. 159
0.45
0.40
Sta. 169
0.49
0.52
Sta. 182
0.48
0.48*
I-T
0.69
0.65
0.29
0.5 1*
0.56
0.46
0.60
0.59
0.51
0.68
by time zero).
often yielded intercepts (i.e. appreciable cumulative uptake at time zero) which for Sta.
2 and 3 were close to 1 ,umol kg-l (see also
the mentioned initial value at Sta. 1). Actually, cumulative NO3 uptake at time zero
is zero by definition; such erroneous intercepts lead to lower calculated rates of cumulative uptake and, hence, division rates
(Banse 199 1, table 2). Note that Martin et
al. (1990a) estimated the community division rates under the assumption that the
decrease of NO3 was linear in time and, by
implication,
that linear algal growth prevailed. Their figure 2, however, shows exponential time changes for NO3 and Chl, as
do my semilog plots.
As stated by Martin et al. (1990a), all
(P < 0.05)
treatments differ significantly
from the controls (Table l), i.e. Fe addition
enhances division rates. Since I use parametric statistics in spite of the small number
of points, the significance level of the enhancement shown is apt to be overestimated (cf. Sta. 1; perhaps also Sta. 3). My reevaluation (Table 1) of the data of de Baar
et al. (1990; see also Buma et al. 199 1) fully
supports their interpretations: Growth rates
in controls are high, but Fe addition can
enhance division rates further (see also next
section).
Note: Dugdale and Wilkerson (1990) in their reevaluation of the data of Martin et al. (1990~~)
emphasized the Chl-specific uptake rates of NO,.
On the basis of a model involving several assumptions (e.g. conversion factors), they found
no significant difference between controls and
treatments and, thus, did not agree with, Martin
et al. (1990a). However, I wish to advise caution,
since my more straightforward, hence parsimonious, approach yields ambiguous results regarding Chl-specific uptake rates. Dividing the predicted NO, uptake for 1 d (from regressions, cf.
Table 1, Martin et al. 1990a data) by the mean
pigment content during that day, after multiplying the initial pigment of that day by [exp(pCLI)
l]lk.t, (with t = l), yields satisfactory ratios [in
pmol N (pg Chl x d)-‘1 of 0.77 and 0.66 for the
controls and 0.90 and 0.66 for the treatments for
days 2-3 and 7-8 at Sta. 2; these may or may not
be indistinguishable. At Sta. 4, however, the ratios vary greatly with time even within treatments
becausethe slopes (exponents) differ greatly among
the NO, and pigment regressions; such variation
within a flask is not to be expected with ordinary
exponential growth.
Rates in Fe-poor ofshore areas and coastal waters- For comparing the averages of
Chl- and NO,-based division rates from
bioassays with the coastal data, it is appropriate to use the range between bulk population and community division rates (from
Fig. 2). Figure 3 shows that on average, di-
vision rates in the controls of the bioassays
from subantarctic and subarctic ojfshore wa-
Phytoplankton division rates
1893
A
ters are about as high as ratesfrom the coastl.5' '
' I"' ' al-andpresumably
Fe replete-stations depicted in Fig. 2, once temperature is
accounted for. Therefore, community
division rates do not appear to be severely
1.0
idepressed throughout seas that are remote
-0
from sources of iron dust, as they would if
the phytoplankton
dominating in situ were
.-I5
Fe deficient. Fe addition, however, regularly
cl 0.5
enhances division rate. The increase is USUally not significant stati‘stically (Banse 199 1;
de Baar et al. 1990; Cullen et al. 1992; Table
1). Some low rates in the controls are ac1
0
2v
10
12 "C
-2
companied by low rates in the treatments
so that, presumably, temperature or Fe were
ca.13
h
16 ca.16
not the only rate-controlling
factors.
Fig. 3. Division rates from bioassays as dependent
Overall, the stations from the Scotiaon temperature, with the “standard curve” for optimal
Weddell Seas with concentrations
of dis- growth (Eppley 1972), half of this maximum (broken
solved Fe of 2-4 nM (de Baar et al. 1990) curve), and the relations for community division rate
(thin line in Fig. 2) and bulk population division rate
did better than those from the presumably
line in Fig. 2) added. Estimated daylength (h)
Fe-poor Ross Sea (Fig. 3; both based on (dashed
shown below temperature scale. Averages for Chl- and
16-h days); the effect of Fe addition was NO,-based rates near 0°C from Table 1, above 10°C
relatively small in the Scotia-Weddell Seas from Banse (199 1). Controls (open symbols) and cor(Table 1). Ironically,
among the four sta- responding treatments (highest Fe additions; filled
symbols) aligned. Circles based on de Baar et al. 1990
tions of Martin et al. (1990a) the highest
(temperature estimated, some symbols offset for clarrates in the controls were found at the pre- ity);
inverted triangles near 0°C based on Martin et al.
sumably most Fe-deficient site (judging from
1990a (some symbols offset for clarity), above 10°C
the location); it was at this station, though,
based on Martin et al. 1989 (temperature estimated).
See also 26°C value for Cullen et al. (1992) in Fig. 2.
that Fe addition had the greatest absolute,
as well as percentage effect (cf. Fig. 3, inverted triangles at - 0.5”C). Other evidence
also suggests that the rate of in situ community division at the station was not de- Low abundance of diatoms and
community division rates
pressed by severe Fe limitation:
Dugdale
and Wilkerson (1990) here estimated a high
This section reviews and discusses the occurrence and role of rare phytoplankton
specific NO3 uptake rate ( VNO~). Further,
I note that the observed removal of 3.7 pmol
species in the offshore areas under considNO3 kg-l in the control, multiplied with a eration. Recall that a feature of the three
molar C : N ratio of 6.6 and a molar C : Fe ocean regions is the low abundance of largeratio of 20,000 (from Martin et al. 1990a)
celled species, although many such species
suggests a consumption of dissolved Fe of occur. The predominance of small cells has
1.2 nmol kg-l. Elsewhere in the Antarctic,
been established by microscopical
counts
Martin et al. (1990b) observed near-surface
(usually of samples of a few up to - 100 ml)
values about a tenth as high. Evidently, more
and by size fractionation of photosynthetic
Fe was available to the plankton than was rate determinations (at most a few hundred
measured as dissolved, which I already notmilliliters) or chlorophyll (usually < 1 liter).
ed for the Gulf of Alaska (Banse 199 1). This
In experiments with contained water in the
conclusion holds even if the C : Fe ratio was
Gulf of Alaska, including the treatments of
a few times higher than assumed above. Note
the Fe enrichments, though, medium-sized
finally that the average division rate of the cells tend to become abundant after - 1 week
equatorial community in Fig. 2 (diamond
of enclosure (Frost 199 1; see Cullen et al.
at 26”C, from Cullen et al. 1992) is remark1992 for the same phenomenon in enrichably low; division rates for controls and ment experiments in the equatorial Pacific).
treatments were similar.
Further, in the central Gulf of Alaska, the
1894
Banse
assemblage of diatoms collected in sediment traps (with a number of large-celled
species prominent and with marked differences among seasons, Takahashi et al. 1990)
is quite unlike that observed in routine
plankton counts from the euphotic zone.
Obviously, large cells are more likely to be
present in settling material than small ones,
but the point here is that these large species
are rare in the surface layers. Finally, in a
central Pacific section from 33”N to 41’S,
Semina (1962) compared l-liter (!) bottle
samples with hauls by nets of 180-pm mesh
size made on the same stations. At the three
stations near the equator, 2, 13, and 4 species of the totals of 29, 82, and 46 species,
respectively, were common to both gears;
at the two southernmost stations, no species
were common among the totals of 26 and
12, respectively. The total specimen numbers of the rare forms collected by the
(coarse!) net in the upper 100 m were rnostly
5 1 liter-l, the maximum at the equator
being 6 liter-l (Semina 1963).
Are many of these uncommon species rare
because of Fe deficiency, which is apt to be
felt more strongly by large than small cells
(Hudson and Morel 1990), or because of
grazing by large zooplankton? Would they
remain rare after Fe fertilization (see Cullen
199 1; Frost 199 l)? Has, instead, the rarity
of large cells (as contrasted with mediumsized forms) in the available Fe enrichments
to do with too small inoculum sizes, or with
Fe- and size-dependent growth rates, or is
it a fluke because of too rare experiments?
Varying plankton composition may also
underlie other observations made during Fe
enrichment work. The community division
rates in controls and treatments at former
weather station “Papa” in the central Gulf
of Alaska by Martin et al. ( 1989; see Banse
199 1) were low relative to expectation from
temperature (Fig. 3, inverted triangle at
12”C), suggesting appreciable limitation by
other than macronutrients. At and near the
same site, the average community division
rate (derived from Chl change, Welschmeyer et al. 1991) of 0.36 div. d-l in 109 in situ
incubations of 24 (48) h, through much of
the euphotic zone during several summers,
was even lower than in Martin’s experiments (in the latter, the rate was usually
determined for periods starting after days 1
or 2, see Banse 199 1). At “Papa,” an important cause for a low rate of commun.ity
division may be the low abundance of diatoms: the division rates from the increase
in the diatom pigment fucoxanthin are much
larger than the community division rates in
the same samples (Strom and Welschmeyer
199 1; Welschmeyer et al. 199 1). It appears
that the rapid intrinsic growth rate of diatoms, coupled in the bottles with reduction
of grazing pressure on these usually larger
cells (demonstrated by Strom and Welschmeyer 199 1; see also Buma et al. 199 l),
tends to lead to their dominance in the treatment bottles after a few days. Thus, the Fe
addition prevents early termination of biomass increase (Banse 199 1, and below) and
may affect division rate differentially among
species.
Elsewhere, the small in situ biomass of
diatoms may be a reason for the low division rates of the equatorial community (diamond in Fig. 2 at 26°C; controls and treatments were indistinguishable).
A similar
depression of community division rate may
be expected for many sites in the Antarctic
where, apart from blooms in the marginal
ice zone, small cells other than diatoms can
prevail. In fact, the community
division
rates at Sta. 145 and 159 (Table 1; at the
same offshore location) are lower than the
net population growth rates of most individual diatom species (from Buma et al.
199 1, table 3) in the same containers. Buma
et al. (1991) already noted differences in
grazing pressure on diatoms and other phytoplankton on the basis of independent evidence. For none of these SiO,-rich offshore
areas is it clear why the abundance of diatoms is low to begin with, although, as stated, many species occur in low abundance.
Discussion
This paper shows that the division rates
of phytoplankton
in Fe-depleted offshore
waters are not low, but most are about as
high as observed in coastal waters where Chl
concentrations
can be large. For both
regions, it is not known whether the high
division rates are Fe saturated, but. a comparison of Figs. 2 and 3 with Eppley’s (1972)
maximal rates demonstrates that even the
Phytoplankton division rates
1895
the low Si : N ratios of surface water, which
low ones are not as depressed as they would
be if Fe were really scarce. Instead, as stated were mentioned earlier, suggest that effects
by Banse (1991), the bioassays from sub- like new CO, fixation may not be predictable everywhere based simply on consumparctic and subantarctic waters suggest that
tion of all excess N. Also, since SiO, has
in situ grazing prevents the doubling or quabeen depleted first, I wonder whether many
drupling of Chl concentrations over ambient levels, which is normally observed in large cells other than diatoms, or only small
flagellates, can be expected; small cells are
the controls; enough Fe is available from
apt to enter microbial food webs that do not
the outset, or is supplied during the interval
lead to high vertical fluxes of organic matter.
of l-2 cell divisions, to permit a material
Moreover, in surface waters where SiO, exincrease of Chl in the controls. Fe addition
in the treatments, however, results in large haustion occurs first, one consequence might
blooms and NO, exhaustion. At the same be that diatoms settling out at the end of
blooms would consume SiO, below the eutime, the phytoplankton
species composiphotic zone and the nitracline and carry it
tion in the treatments tends to change markedly. Basically the same conclusion has been to great depths, which might be a regular
feature in the Barents Sea (Rey and Skjoldal
drawn for the waters of the eastern equa1987). If so, the Si04 supply to the surface
torial Pacific (Cullen 199 1).
in subsequent years would be affected unThe hypothesis of Fe limitation
of phytoplankton growth in large parts of the sea favorably.
Lessons for bioassays-The Fe enrichis currently being discussed on the basis of
ment experiments published so far did not,
an experimental data set, which is unusually
small for this major issue and which has not by their design, measure rates of cell dividivision, because
answered several questions. On the as- sion but of community
were always enclosed
sumption that more bottle experiments on small zooplankton
with phytoplankton; the bioassays dealt with
community
and especially population division rates are called for prior to field ma- one equation with two unknowns (Eq. 2).
nipulation, this discussion emphasizes les- Further, to derive instead the instantaneous
growth rate of phytoplankton
and, hence,
sons from algal cultures and published
division rate from the cumulative NO3 upbioassays.
take can serve only as a substitute for direct
Lessonsfor the fild from algal cultures Figure 2 extends to field data the great role measurement because the calculation
is
of temperature
summarized
by Eppley
heavily affected by the quality of the initial
(1972) for division rates in algal cultures. In NO3 determinations
(Banse 199 1). Other
consequence, when comparing the three
criticism, which can be advanced against
major ocean regions and thinking of field
the available assays, concerns the exclusion
manipulations
with Fe, algal growth proof large zooplankton from the containers
cesses must be expected to proceed 2-3 times
because of low abundance. This omission
faster in equatorial waters than in the sub- will shift the competitive advantage in the
arctic Pacific during summer and 5-6 times
bottles toward the larger algae directly;
faster than near an ice edge. In contrast,
moreover, as noted by Buma et al. (199 1)
physical processes like advection and eddy for Antarctic plankton, it will have the same
diffusion will be largely independent of temeffect indirectly by reducing grazing presperature. Because of small seasonal change,
sure on the small animals that prey on the
temperature in each of the three regions will
initially
dominant
small phytoplankton.
matter little for division rates, although it Again, more than one unknown is present
may affect changes of assemblage compoin the equation to be solved by the enrichsition and, thus, indirectly influence diviment experiments. I believe, however, that
sion rates (e.g. via cell size).
even so, several outstanding questions in
Further, in respect to large-scale experithe Fe controversy can be addressed by difments with Fe additions in the Southern
ferently designed bottle assays.
Ocean, the high half-saturation constants for
Proximally at issue for understanding the
SiO, uptake by some dominant diatoms and high-nutrient,
low-chlorophyll
paradox is
1896
Banse
how small or large p may be in situ, whether
toms?) flourish in assays because of removal
large cells (or diatoms as a whole) are usu- of Fe deficiency” vs. “they do so because of
ally Fe limited while small cells are not, and absence of suitable grazers,” can be examhow even a small p is balanced by grazing
ined from bottle experiments by the process
and physical processes so that the local time
of elimination. If the former statement does
change is close to zero. The biological issues not hold, the latter can well be true. Cumneed to be seen in the framework of Eq. 3, bersome as such species-specific approaches
with p and m varying among species. Among
will be for the individual
researcher, much
the questions that can be addressed with
less manpower and funds will be required
small containers on shipboard are: where, than for a manipulation
of an area in the
when, and to what degree does Fe addition
open sea where grazers are present in notenhance the division rate of the dom.inant
controllable numbers and kinds. The bottle
phytoplankton
species vs. the stimulation
experiments can be done first and soon, but,
of rare, larger species that might require
most importantly,
they will yield less amhigher concentrations
of Fe? what effect biguous results than the field manipulation
does the reduction of grazing by larger an- because of better definition of conditions
imals, which are normally excluded from
before and during the incubations, includbottles, have on the enhanced population
ing rigorous control experiments and repgrowth of small predators, which depress lication, and the absence of eddy diffusion
the abundance of their prey (i.e. of the phyand advection.
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