Download FROST, BRUCE W. The role of grazing in nutrient

Limnol. Oceanogr., 36(8), 1991, 1616-1630
Q 199 1, by the American
Society of Limnology
and Oceanography,
Inc.
The role of grazing in nutrient-rich areas of the open sea
Bruce W. Frost
School of Oceanography, WB- 10, University of Washington, Seattle 98 195
Abstract
No single factor accounts fully for the persistently low phytoplankton stocks in the nutrient-rich
areas of the open sea. However, grazing plays the necessary role of consuming phytoplankton
produced in excess of losses due to physical processes and sinking. Without grazing, even if specific
growth rate of the phytoplankton is less than optimal for the prevailing light and temperature
conditions, as might be so under limitation by a trace nutrient such as Fe, the phytoplankton stock
would still accumulate with attendant depletion of nutrients. Observations during spring and
summer in the open subarctic Pacific argue against limitation of phytoplankton growth to the point
where phytoplankton stock could not increase in the absence of grazing. An ecosystem process
model of the phytoplankton-grazer interaction suggests that two processes-grazing control of
phytoplankton stock and preferential utilization of NIH, by the phytoplankton-are sufficient to
explain the continuously low phytoplankton stock and high concentrations of macronutrients.
However, the grazing control may be exerted on a p:hytoplankton assemblage structured by Fe
limitation. In particular, the intrinsic growth rates of potentially fast-growing diatoms seem to be
depressed in the open subarctic Pacific. These conditions probably apply to two other nutrientrich areas of the open sea, the Pacific equatorial upwelling region and the subantarctic circumpolar
ocean, although in the latter region light limitation of phytoplankton growth may be more severe
and silica limitation may influence the specific composition of the phytoplankton assemblage.
Realization
that grazing zooplankton
could control the abundance of phytoplankton in the sea dates back over half a century
to the studies of the Kiel and Plymouth
plankton study groups (Mills 1989). Inspired by Fleming’s (1939) analysis, Riley
(1946, 1947) formulated the first mathematical model describing the dynamics of
phytoplankton and grazer assemblages, and
quantitatively
demonstrated the potential
capability of grazers to maintain low stocks
of phytoplankton.
Recent reviews (Frost
1980; Raymont 1980) stressed the likely
major impact of grazing as implied by models, but also noted the need for corroborative field measurements of phytoplankton
mortality rates due to grazing.
Possibly because grazing mortality of entire phytoplankton assemblages has been so
difficult to measure in the ocean, and cer-
tainly because of recent rediscovery of the
“microbial loop” containing a host of previously relatively unknown grazers whose
study has required new methodology, the
magnitude of grazing rates is not well established for most marine pelagic systems,
especially those of the open sea. Consequently, several hypotheses besides control
by grazing are potentially alternative explanations (e.g. Cullen 199 1) of the phenomenon under discussion in this symposium,
namely, that in surface waters of several
large, open-ocean areas concentrations
of
phytoplankton
are perpetually low despite
high concentrations of macronutrients.
My view is that none of the hypotheses
really are alternatives in the sense of being
mutually exclusive explanations of the phenomenon, but all implicate processes that
may simultaneously contribute, in differing
degrees, to produce it. In this paper I demonstrate the argument by assessing the imAcknowledgments
pact of grazing relative to other processes
I thank B. C. Booth, J. N. Downs, D. L. Mackas, C.
controlling
phytoplankton
13.Miller, S. Tabata, N. A. Welschmeyer, and P. A. potentially
areas
Wheeler for providing data; special thanks to C. B. abundance in the large, nutrient-rich
Miller for many useful discussions of subarctic Pacific of the open sea. To make the argument
plankton dynamics.
quantitative I emphasize observations at the
Research supported by NSF grants OCE 86- 1362 1 former Ocean Weather Station P (5O”N,
and OCE 89-17671.
145”W) in the Gulf of Alaska. However, I
School of Oceanography, University of Washington,
note points of similarity or dissimilarity with
Contribution 1923.
1616
1617
Grazing in the open sea
two other large, nutrient-rich
areas of the
open sea- the Pacific equatorial upwelling
region and the circumpolar subantarctic region.
Annual cycle of phytoplankton and NO3
in the open subarctic Pac$c
Based on the quantity of Chl a integrated
over O-50 m, there is virtually no seasonal
variation in phytoplankton
standing stock
at Station P (Fig. IA). This seems to apply
throughout the open subarctic Pacific (Frost
1987; Sambrotto
and Lorenzen
1986).
Clearly there is temporal variability in phytoplankton stock at Station P, but it is constrained within fairly narrow bounds; for
the entire data set integrated Chl a ranges
over a factor of only 8. The narrow range
of variation contrasts with observed strong
seasonal fluctuations
of phytoplankton
abundance, reaching bloom concentrations
with attendant nutrient depletion, in the
shelf waters (e.g. Landry et al. 1989; Denman et al. 198 1) and inland coastal waters
(e.g. Kanda et al. 1990; Parsons et al. 1970)
bordering the open Gulf of Alaska. In Dabob Bay, Washington, the phytoplankton
stock range seasonally over a factor of 67
(Fig. 1B). The same contrast, with less intensive and complete seasonal coverage, is
evident between waters of the deep basin
and the broad continental shelf in the eastern Bering Sea (e.g. Sambrotto et al. 1986).
The much more substantial seasonal variability of phytoplankton abundance in shelf
and coastal waters and its cause are important topics to which I return later.
At Station P, the seasonally relatively
constant phytoplankton
stock exists despite
strong seasonal variation in properties of
the physical environment that can have significant impact on the specific growth rate
of the phytoplankton
(Fig. 2). Growth conditions for the phytoplankton are surely very
different, for example, between winter and
summer. This is suggested by the annual
cycle of NO3 (Fig. 3), which shows a distinct
seasonal cycle (buildup in winter, drawdown in summer) in the surface layer. Notice, however, that NO, is not depleted in
summer-a
feature of the entire open subarctic Pacific (Anderson et al. 1969).
Though seasonal coverage is much less
A. Station P
G
200
'a
a 150
85
u O 100 I
0
60
120
180
240
300
360
B. Dabob Bay
400
I
-0
60
120
180
240
Day of Year
300
360
Fig. 1. A. Phytoplankton standing stock (as Chl a)
observed in the vicinity of Station P. Data cover all
seasonsduring the years 196l-l 967 (Frost et al. 1983)
and 1980-l 98 1 (Clemons and Miller 1984), and cover
late spring-early summer and late summer-early fall
during the SUPER cruises, 1987-l 988 (N. A. Welschmeyer pers. comm.). B. As panel A, but for Dabob Bay,
Washington. Data for the years 1979 and 1982 (Frost
1985), 1985-1986 (Frost 1988), and 1990-1991 (B.
Frost and J. Downs unpubl. data).
complete, the subantarctic circumpolar waters are in some respects similar to the open
subarctic Pacific. Concentrations
of Chl a
in the mixed layer are always low and in the
range reported for the open subarctic Pacific
(Fukuchi 1980). On the other hand, although NO3 is high, SiO, is low in surface
waters (Kamykowski and Zentara 1985; van
Bennekom et al. 1988). Although growth
conditions for the phytoplankton
must also
be seasonally variable in the subantarctic
circumpolar
region, mixed layers can be
deeper in summer than in the open subarctic
Pacific (Levitus 1982; Foster and Middleton
1984). In regions of strongest upwelling in
the equatorial Pacific, concentrations of Chl
a and macronutrients are similar to those
at Station P (Chavez et al. 1990). However,
seasonality of growth conditions must be
.
1618
Frost
60
-
0
120
0’
I
I
I
0
60
,
1
I
120
180
240
Day of the Year
I
300
-4
360
Fig. 3. Concentration of NO, in the upper 20 m at
Statton P, 1966-1976 (adapted from Parslow 198 1).
Curve is a Sth-order polynomial fitted by least-squares
to the data.
Day of Year
Fig. 2. Some physical properties at Station P in
1970. Data from Dep. Transport, Meteorol. Branch,
Canada (I 97 1) and from a magnetic data tape provided
by S. Tabata.
much reduced compared to the subpolar
open seas.
It was for many years presumed that in
the open subarctic Pacific grazing zooplankton keep phytoplankton stocks low, thereby
preventing depletion of macronutrients
in
the surface layer (see Miller et al. 1988; Parsons and Lalli 1988). Indeed, models demonstrate that such a role for grazing is plausible (Evans and Parslow 1985; Frost 1987
in prep.). Yet an alternative proposal (Martin et al. 1989) that Fe limitation
of phytoplankton growth is somehow responsible
for low phytoplankton
stocks and high nutrients indicates that the specific mechanisms need to be re-examined.
Here, I treat the observations from Station P in two ways. First, I make a quan-
titative assessment, leading to an inescapable conclusion, of the relative magnitude
of processes that must be at work to maintain the low, relatively
constant, phytoplankton stock, for this seems to be the essence of why the open subarctic Pacific is a
nutrient-rich
area that never exhibits phytoplankton blooms. The argument appears
to be generic for the nutrient-rich,
open
ocean areas, as I show.. I then present the
results of a model illustrating a possible dynarnical relationship between phytoplankton and grazers.
Control of phytoplankton standing
stock in the open subarctic Pacific
Daily observations of Chl a concentration
at Station P exhibit the same pattern as the
seasonal data (Fig. 4). There is daily variability, but it is constrained. These data imply that the local rate of change of phytoplankton stock averages out very close to
zero on a time scale of several days to a
week or two. The local rate of change of
phytoplankton stock (P) depends on several
processes
ap =
at
-
growth - advection,,,,,
+ diffusion.,,,, - sinking
- grazing.
(1)
Although all the necessary measurements to
evaluate Eq. 1 have not been made simultaneously at Station P, it is nevertheless possible to estimate the relative magnitudes of
the terms for specific time periods.
c
1619
Grazing in the open sea
1
0020’
Chl
o.oI
7
11
19
23
15
Day in May 1988
a
(mg m-3)
31
27
iO”O0’
Fig. 4. Short-term temporal variation in surface
Chl a at Station P in May 1988 (data provided by N.
A. Welschmeyer).
Estimates of phytoplankton standing stock
and production rate were made during a
cruise of the SUPER (Subarctic Pacific Ecosystem Research) investigation to Station P
in May 1988. Using these data, I calculated
finite specific growth rates for the phytoplankton assemblage in the mixed layer (Table 1). The mean finite specific growth rate
was 0.57 d-l; the corresponding instantaneous growth rate (In 1.57) is 0.45 d-l (or
a doubling time of - 1.5 d). This growth rate
is based on measurements of phytoplankton
production rate, and it is assumed, of course,
that phytoplankton
production rate measured by in situ incubations
represents
Table 1. Phytoplankton standing stock as Chl a (2
Chl a, mg Chl a m-2) and C (ZC, mg C mm2),phytoplankton production rate (PP, mg C m-2 d-l), and derived finite specific growth rate (PKX, d-‘) for the
phytoplankton assemblage at Station P in May 1988.
PP based on 24 or 48 h in situ incubations (dawn to
dawn). Standing stocks and production rates are integral values for the mixed layer (Z,?,,m). Data provided
by B. C. Booth and N. A. Welschmeyer.
May
Zn
Xhl
8
11-12
14
17-18
20
22
27
80
60
60
60
60
80
70
23.6
16.6
23.3
18.7
22.6
15.6
12.3
a
ZC*
1,258
885
1,242
997
1,205
831
656
PP
PP/ZC
368
0.29
424
0.48
694
0.56
606
0.61
506
0.42
806
0.97
425
0.65
mean = 0.57
(SE = 0.10)
* Estimated from Xhl
a x y, where y is mean C:Chl
a (53.3, SE =
2.3, N = 31) based on microscopical
analysis of total phytoplankton
assemblage (method described by Booth et al. 1988) for vertical profiles
on 8, 14, 20, and 21 May.
19”40’
145’20’
145”OO’
144’40’
Fig. 5. Spatial variation in surface Chl a on a 50
x 50-km grid centered on Station P (5O”N, 145’W),
14-15 May 1984. Based on a continuous record of
chlorophyll fluorescence obtained from a pumped seawater flow (at -3-m depth); survey was done in 30 h.
Figure provided by D. L. Mackas.
something close to net rate of formation of
organic matter in situ by the phytoplankton.
To evaluate
relative
magnitudes
of
changes in phytoplankton
stock due to horizontal advection and difhtsion, I utilize data
from a spatial survey done at Station P on
14-15 May 1984 (Fig. 5). Again using Chl
a as a measure of phytoplankton stock, the
horizontal gradient of phytoplankton
stock
west of Station P (i.e. directly upstream of
the station) was on the order 0.01 mg Chl
a mm3 km-l. Given mean eastward geostrophic currents of 5-l 0 cm s-l (4-9 km
d-l; Favorite et al. 1976), the change due to
horizontal advection would be 0.04-O. 1 mg
Chl a m-3 d-‘, which is an appreciable daily
change, equivalent to - 1O-20% of the mean
phytoplankton
concentration
in Fig. 5.
However, the horizontal gradients of chlorophyll are neither regular nor fixed in space
(cf. gradients east and west of Station P in
Fig. 5), and there is not a consistent larger
1620
Frost
scale upstream gradient farther to the east
of Station P (Sambrotto and Lorenzen 1986).
Thus, over a 5-10-d period the change due
to advection at Station P must average out
close to zero.
With regard to vertical advection, Station
:P is in a region of divergence, with a very
slow rate of upwelling (15-20 m yr-I; Favorite et al. 1976), so vertical advection is
negligible on a time frame of several days
to a few weeks.
The mean change in horizontal gradient
of Chl a in Fig. 5 is -0.01 mg Chl a m-3
kmm2. With a likely magnitude for horizontal eddy diffusivity (1 O5cm2 s-l), the change
in chlorophyll
concentration
due to horizontal diffusion must be very small (order
0.01 mg Chl a m-3 d-l, or a few percent of
the phytoplankton
stock per day).
Finally, with the range of maximum vertical gradients of Chl a just below the mixed
layer (0.003-0.023 mg Chl a m-3 m-l, based
on seven vertical profiles in May 1988; N.
A. Welschmeyer pers. comm.) and a probable range for vertical eddy diffusivity just
below the mixed layer in May (3-8 cm2 s-l,
Anderson et al. 1977), changes in phytoplankton stock due to vertical exchange between the mixed layer and the layer below
ranged from 0.5 to 7.9% of the mixed layer
standing stock per day.
Taken together, diffusion and advection
are likely to produce a net negative local
change in phytoplankton stock in the mixed
Layer that might be up to 10% d-l, but usually less. Although such physically induced
changes could account for a significant part
of the day-to-day variability in Fig. 4, they
could not account for the month-long maintenance of phytoplankton
stock within the
narrow range observed, given a mean specific growth rate of 0.57 d-l (Table 1).
The phytoplankton assemblage at Station
P is dominated by pica- and nanoplanktonsized cells (Booth 1988) which probably explains the relatively small sinking losses of
phytoplankton
(on average, -2% d-l of the
phytoplankton
stock in the mixed layer;
Miller et al. 1988; N. A. Welschmeyer pers.
comm.).
Staying with finite daily rates of change
and combining the advection and diffusion
terms in Eq. 1, we can summarize the pro-
cesses causing change in phytoplankton
stock for May 1988:
g
= (0.57 - 0.10 - 0.02 - g)P
(2)
where g represents the specific grazing mortality rate. Thus
$
= (0.45 - g)P.
Clearly, for APlAt to have been about zero
at Station P over a period of several weeks
in ‘May 1988 (Fig. 4) the finite grazing loss
must have been a substantial
fraction
(- 80%) of the specific growth rate and must
have been -0.45 d-l. One objective of the
SUPER investigation was to directly assess
gra.zing, and some results are presented elsewhere (Miller et al. 199 1; the experimental
estimates of grazing in May 198 8 were of
the: necessary magnitude to balance phytoplankton growth, and both rates were similar to the rates obtained by my analysis.
Such calculations can be made for other
seasons at. Station P, but no other comprehensive data set comparable to that of May
1988 exists. Nevertheless, it is worth noting
that during the last SUPER cruise (5-25 August 1988), alternating between Station P
and a station at 53”N, 145”W, the mean
specific growth rate of the phytoplankton,
calculated as outlined in Table 1, was 0.44
d-” (SE 0.035, N = 7). The value is lower,
but not statistically significantly different,
than that for May 1988 (Table 1) due to a
larger C : Chl a ratio (87.3, SE 5.3, N = 17;
B. Booth pers. comm.). Phytoplankton
stocks did not change significantly at either
station during the cruise. Thus assuming the
same fractional losses of phytoplankton
to
advection, diffusion, and sinking estimated
above, for APlAt to be zero in a phytoplankton assemblage growing at 0.44 d-l the specific grazing mortality rate must be -70%
of the phytoplankton
specific growth rate.
ThLese two rates were also in the range of
those estimated experimentally
in August
1988 (Miller et al. 199 1).
.4pplication of a phytoplankton
pigment
budget at Station P suggests that the grazing
is due chiefly to very small (microzooplankton) grazers (Miller et al. 1988; N. A.
Wlelschmeyer pers. comm.), which is con-
1621
Grazing in the open sea
sistent with the dominance of the phytoplankton at Station P by pica- and nanophytoplankton,
as noted earlier.
The conclusion that grazing mortality rate
must be a substantial fraction of the phytoplankton specific growth rate can also be
drawn for the other two nutrient-rich,
openocean areas under consideration here. For
the Pacific equatorial upwelling region a
more significant vertical advection term
must be considered, with advective loss of
phytoplankton
stock due to divergence at
the equator, but, with the observed vertical
velocities (1 or 2 m d-l; Philander 1990)
and a mixed-layer depth of 30 m, it must
be a very small loss-a few percent per day
at most. Cullen et al. (in press) and Pena et
al. (199 1) also concluded that grazing must
control phytoplankton
stock in the Pacific
equatorial upwelling region. In open subantarctic waters, light limitation might be a
more severe constraint on phytoplankton
growth than in the subarctic Pacific because
of substantially deeper mixed layers in summer (Levitus 1982). In both regions the
dominant grazers are also likely to be microzooplankters,
since the phytoplankton
assemblage is dominated
by pica- and
nanophytoplankton
(Hewes et al. 1985;
Probyn and Painting 1985; Chavez et al.
1990; Pefia et al. 1990).
10 1
I
I
867
k
~6-
0
5
10
15
DAYS
Fig. 6. Increase in phytoplankton stock (initially at
0.2 mg Chl a m-3) projected for different net specific
growth rates (d-l) with no grazing.
in grazer populations (Cushing 1959). Protozoans are not the types of grazers envisaged by Walsh (1976) nor would his proposed effect of frequency of variability
of
the physical environment
explain the persistent balance in the open subarctic Pacific,
where intense storms are frequent. Nevertheless, as reframed above, the hypothesis
can be the basis for observational and experimental tests.
Postponing discussion of episodic forcing
events- to the next two sections, I have
graphed the expected increase in a phytoplankton assemblage in Fig. 6, given different net specific growth rates and no grazing
mortality, from an initial concentration of
Grazing hypothesis
0.2 mg Chl a m-3 (i.e. the initial concentraThe analysis leads to a general hypothesis,
tion observed at Station P in May 1988: Fig.
modified and extended from that of Walsh
4). If, as in May 1988 (Table I), the net
(1976), about the role of grazing in the nuspecific growth rate of the phytoplankton
is
trient-rich areas of the open sea. In the nu- 0.37 d-’ (the equivalent instantaneous net
trient-rich areas ofthe open sea,phytoplankspecific growth rate from Eq. 3), then with
ton net spec& growth rate and spec$c no grazing a phytoplankton
bloom would
grazing mortality rate tend toward approx- develop in a matter of 8-10 d (heavy line
imate balance that may be perturbed, but in Fig. 6). Naturally, if a bloom occurred
not fully disrupted, by episodic forcing events nutrients would be depleted. For the phyexternal or internal to the pelagic food web. toplankton stock to remain essentially unNet specific growth rate of the phytoplankchanged over 3 weeks as observed (Fig. 4),
ton is defined here as the specific growth
the specific grazing mortality rate must be
rate adjusted for losses due to physical provery near 0.37 d-l. Such grazing would not
cesses and sinking, but not grazing. The balonly keep the phytoplankton
stock low, but
ance is possible because the dominant graz- would also indirectly prevent macronutriers are very probably small heterotrophic
ents from being depleted.
protists, whose growth rates can equal or
The other two curves in Fig. 6 are meant
exceed those of their phytoplankton
prey,
to extend the range of possible net specific
greatly reducing time lags between increase
growth rates to phytoplankton
assemblages
in phytoplankton
abundance and increase
subjected to greater constraints on their in-
1622
Frost
Herbi wrous
Microzooplankton
I n‘%w
-hi
5
I
Phytoplankton
”
minipellets
.Irn
f
q2
I
4
I
NO3
4
I
6
*
.r,
----
NH4
[ Pr-;t;fJ..in]
/
b
&
-HH
911
Fig. 7. Trophic interactions represented in the model. Solid lines are phagotrophic links; broken lines are N
recycling links [q,, fraction of herbivore mortality released as NH,; q2,fraction of herbivore egestion (“minipellets”) released as NH& dashed line represents input of NO, by vertical turbulence and entrainment.
ttinsic growth, such as might be imposed
by more severe light limitation in the subantarctic region due to deeper mixed layers
or by scarcity of a trace nutrient, such as
soluble Fe, as has been suggested to occur
in the nutrient-rich
areas of the open subarctic Pacific and subantarctic seas (Martin
et al. 1989, 199Ob).Note, however, that even
at the low net specific growth rate of 0.1 d--l,
which must be well below the observed values for nutrient-rich
open sea areas, at least
in summer (Banse 199 l), the phytoplankton
stock would still quadruple in just 2 weeks
and increase by 20 times in a month, if grazing did not consume the daily production
remaining in excess of other losses. There
must be a removal of excess phytoplankton
production by grazing in all three nutrientrich areas considered here; limitation
of
phytoplankton
growth, by either light or a
trace nutrient such as Fe, is not sufficient as
the sole explanation of those areas of the
open sea where nutrient concentrations are
persistently high and phytoplankton
stocks
are low. Even if the specific growth rate of
the phytoplankton
assemblage is less than
optimal, grazing must still approximately
balance phytoplankton
net specific growth
to prevent phytoplankton
blooms and nutrient depletion in the nutrient-rich
areas of
the open sea.
Returning to Station P, the primary production rate data for summer, indicating
malderately high specific growth rates of the
phytoplankton
assemblage, argue against
limitation of phytoplankton
growth, by either light or a trace nutrient such as Fe, to
the: point where phytoplankton
stock could
not increase in the absence of grazing. Thus,
phytoplankton
growth and grazing must be
dynamically closely integrated, particularly
in a seasonally variable growth environment such as the subarctic Pacific (Fig. 2).
Seasonal plankton dynamics in the
open subarctic Pa&&
I[ have used an ecosystem process model
to investigate the dynamic interactions between phytoplankton and grazers in the open
subarctic Pacific. The details of ithe model
and its predictions are described elsewhere
(Frost in prep.), but the model is directly
derived from an earlier version (Frost 1987,
experiment 3) representing the dynamics of
two functional trophic groups: phytoplan kton (pica- and nanophytoplankton)
and their
grazers (phagotrophic
protistan grazers).
Figure 7 schematically illustrates the modeled trophic interactions.
The model is one-dimensional,
with the
ocean treated as a three-layered system 120
m deep (a homogeneous mixed layer, a
1623
Grazing in the open sea
stratified intermediate layer, and the permanent halocline). Stocks of phytoplankton, herbivorous
microzooplankton,
and
two nitrogenous nutrients (NO3 and NH4)
are allowed to vary in the mixed layer and
intermediate layer, but are fixed at 120-m
depth. There is entrainment to and detrainment from surface populations and nutrient
stocks when the mixed layer deepens and
shoals. There is seasonally variable vertical
turbulent mixing (isotropic in the intermediate layer) between the mixed layer and
the layer below. The environmental
forcing
variables (incident solar radiation, mixedlayer depth, and mixed-layer temperature)
are input to the model with daily observations obtained at Station P in 1970 (Fig. 2).
A key feature of the model is the pattern
of nutrient utilization and recycling. Based
on experiments at Station P, Wheeler and
Kokkinakis (1990) concluded that NO3 uptake by the phytoplankton
is inhibited by
the presence of regenerated forms of N,
principally
NH4. Because the mechanism
and exact physiological basis of inhibition,
particularly the dependence on concentrations of the two forms of nitrogenous nutrient, remain obscure (Dortch 1990), a simple contingency rule is used in the model.
It is assumed that phytoplankton
preferentially utilize NH4 and absorb it according
to Michaelis-Menten
kinetics. It is further
assumed that phytoplankton
growth is not
limited by nitrogenous nutrient; any portion
of the N requirement (set by C uptake) not
satisfied by NH4 is met by the uptake of
N03. Other forms of regenerated N (e.g.
urea) are not distinguished from NH, in the
model. A primary source of NH4 in the
model is regeneration by grazers, but this is
insufficient by itself (King 1987), and other
sources of NH4 must be added to produce
realistic concentrations (broken lines in Fig.
7). These include excretion by carnivores
(predators of herbivorous microzooplankton), taken to be a fraction (4,) of daily herbivore predation mortality, and the recycling of a fraction (qJ of the N contained
in fecal material (“minipellets”)
produced
by microzooplankton
grazers.
The model was applied by an essentially
inverse method of fitting to the SUPER data.
That is, grazing, growth, and predation co-
o100
150
o!
100
I
I
I
I
150
200
250
300
Ok
0
60
200
120
180
240
Day of the Year
300
250
300
360
Fig. 8. A. Phytoplankton standing stock (as integrated Chl a) predicted (line) and observed (0) during
the SUPER cruises (1987, 1988). B. Phytoplankton
production rate predicted (line) and observed (0) during the SUPER cruises. Observations provided by N.
A. Welschmeyer. C. As panel A, but for entire year
using data (0) from Fig. 1A.
efficients for the herbivorous
microzooplankton were first selected to give a fit to
Chl a data (Fig. 8A). Then values of photosynthetic parameters were found that produced a fit to observed production rates (Fig.
8B). A major finding was that to simulate
observed levels of phytoplankton
production, maximum intrinsic growth rates had
to conform to the optimal temperature-dependent rates (Eppley 1972); there was no
field evidence that phytoplankton
growth
was less than expected for the prevailing
light and temperature conditions. Given this
fit to the seasonally restricted SUPER data,
1624
m
h
Frost
0
60
120
180
240
300
360
0
60
120
180
240
300
360
20
2
Z
;
$
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z
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.
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60
.
1
120
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180
240
300
360
Day of the Year
Fig. 9. Mixed-layer concentrations predicted by the
model. A. Phytoplankton (P) and herbivorous microzooplankton (H). B. NO, (data from Fig. 3-O). C.
NH,. Vertical mixing and nutrient recycling efficiency
parameterized as for the cases with heavy lines in Fig.
12.
the model predicts an annual cycle for integrated Chl a that is similar to the observed
annual cycle, though not reproducing the
full variability of the observations (Fig. 8C).
The predicted annual cycles for concentration of Chl a and herbivorous microzooplankton
indicate
that phytoplankton
growth and grazing are in balance throughout the year, as evidenced by the continuously low phytoplankton
stock (Fig. 9A),
despite large seasonal changes in growth
conditions (Fig. 2). A wide range of parameter values for herbivore ingestion rate,
growth rate, and mortality produce this general pattern of balanced phytoplankton
growth and grazing (Frost in prep.). Again,
the balance is possible because the modeled
grazer is a protozoan with relatively high
potential grazing and growth rates (Frost
1987). In addition, a fundamental property
of this pelagic ecosystem, first noted by
Evans and Parslow ( 198 5), is that even in
winter positive phytoplankton
production
is possible because the shallow permanent
halocline limits the depth of winter mixing.
This means that herbivores can be nourished and grow in winter, ensuring that a
responsive grazer population
is continuously present. The predicted fluctuations in
stocks of phytoplankton
and grazers (Fig.
9A) are driven by daily variability
in insolation and mixed-layer depth (Fig. 2), although the intensity of the fluctuations can
be amplified by biological interactions, as
illustrated below.
NO, is drawn down in the summer (Fig.
9B), but is not fully depleted because of rapid recycling of N and the preferential utilization of NH, by the phytoplankton
in the
mixed layer. NO3 increases in fall and winter because of the combined effects of declining phytoplankton
production
due to
decreasing insolation, and cooling and destratification of the upper layer, entraining
NO3 from below. NH4 is always low, but
very dynamic (Fig. 9C); its concentration
de:pends on both utilization
by the phytoplankton and the recycling efficiency of the
food web, as illustrated below.
The full range of natural variability is generally not reproduced by the model (Fig. 8),
except perhaps in spring when the upper
water is restratifying. It is useful to look in
more detail at that period, not only because
it illustrates the effect of episodic forcing
events, but also because it suggests some
constraints on tests of the grazing hypothesis. Figure 10 gives predicted and observed
Chl a and NH, concentrations in the mixed
layer for May. Note the predicted fluctuations (Fig. 1OA) that are driven in the model
by rapid changes in mixed-layer depth; variability of the physical environment perturbs
the balance but does not disrupt it to the
extent that a phytoplankton
bloom occurs.
An even larger perturbation
is evident in
early June (Fig. 9A, day 155), driven by
rapid shoaling of mixed-layer depth to only
10 m (Fig. 2). Clearly, there are times when
p‘hytoplankton growth and grazing may not
be in balance or even close to it. Thus, spot
Grazing in the open sea0.7
=
b
0
0.0
A
.
0.6
1625
-
I =- ’ . 1. - - ’ 1 - . - - 1 - * - ’ ’ . . - - ’ . . . * 1
121
126
131
136
141
146
151
MODEL
DAY (MAY)
0.51
0.4 I
0
b
.
0.3
.
0.2
.b
.
.
*~zooo
0
0.1
0
0
b
oo
.
beog
0
0.
0
bob
0
00
00
0
1
6
11
DAY
16
IN MAY
21
1988
26
120
180
240
300
9
360
- Day of the Year
.
. .
60
31
Fig. 10. A. Daily model predictions for mixed-layer concentrations of phytoplankton (0) and NH, (0).
B. Observations of same, at Station P in May 1988.
Data in panel B provided by P. A. Wheeler and N. A.
Welschmeyer.
measurements of grazing and growth may
not be sufficient to test the grazing hypothesis; measurements should be made over a
significant time period, say, on the order of
5-10 doubling times of the phytoplankton
(as was done during the SUPER investigation; Miller et al. 1991).
Two essential features of the plankton dynamics in the open subarctic Pacific are accounted for by this model-the
relatively
low phytoplankton stock and the year-round
high NO3 concentration. First, the predicted
phytoplankton
stock is strongly influenced
by both the modeled feeding behavior of
the grazer and the predation mortality imposed on the grazer (Fig. 11). For a given
value of insolation
the concentration
of
phytoplankton
determines the phytoplankton production rate in this model, as it seems
to do in the ocean as well (N. A. Welschmeyer unpubl. data), which is a strong argument for studying not only the feeding
responses of microzooplankton,
but also
those of their predators. Notice that the
magnitudes of the fluctuations produced by
episodic physical forcing (chiefly change in
Fig. 11. Annual cycle of phytoplankton standing
stock (as Chl a) predicted by the model with different
combinations of herbivore feeding threshold (P,, mg C
m-3) and herbivore maximum specific mortality rate
(g, d-l). Lower curve: P,, = 7.5, g = 0.2; middle curve:
P, = 10.0, g = 0.2; upper curve: PO = 10.0, g = 0.3.
(See equations 18 and 19 of Frost 1987 for context of
parameters in model.)
mixed layer depth) are amplified at high rates
of predation. In fact, predation on the grazers, a process internal to the food web, has
the potential to perturb the balance by itself,
as noted below.
Second, the predicted annual cycle of NO,
depends, of course, not only on the rate of
utilization
of NO3 by the phytoplankton,
but on the rate of vertical mixing and the
nitrogen recycling efficiency of the pelagic
food web (Fig. 12). A steady annual cycle
of NO3 is not easily produced by the model;
NO, concentration at the end of the year
may be higher or lower than at the beginning
of the year, just as observed interannually
at Station P (Parslow 198 1). Parameterization of the vertical and seasonal variation
in mixing rate, especially winter mixing, is
important in the model (Fig. 12A). However, in the ocean a few brief, intense mixing
episodes in winter may be very significant
in establishing the winter NO3 concentration (Large et al. 1985), and such episodes
are not included in the model. To achieve
concentrations of NH, and NO3 similar to
those observed in the mixed layer at Station
P during the SUPER cruises (Wheeler and
Kokkinakis 1990) requires the recycling efficiency (N released by consumers/total
N
Frost
1626
0
0
I
I
I
I
I
I
60
120
180
240
300
360
processes-grazing
and preferential
utilization of NH4 by the phytoplankton-are
sufficient to explain why the phytoplankton
ass,emblage remains continuously rare and
NO3 remains high year-round. It was not
included in the model, so Fe limitation
of
phytoplankton
growth (Martin et al. 1989)
need not be invoked. Nevertheless, before
these conclusions from the model can be
applied to the open subarctic Pacific, two
presumptions about food-web interactions
nee:d to be examined; one of these may indeed involve Fe limitation.
Food- web interactions
%
a
2
0.28
0.19
10
0.13
,
iu"
'5
h
.z
%
I
o!
0
60
120
I
I
I
II
180
240
300
360
Day of the Year
Fig. 12. A. Predicted mixed-layer concentration of
NO3 for different intensities of turbulent vertical mixing (K,, cm2 s-l) in the intermediate layer. Upper line:
case with constant K, (2.0 cm2 s-l); middle line: case
with seasonally variable K,, = ~(0.01Z,,) where Z,, is
mixed-layer depth and K = 2.0 cm2 s-l m-l; lower (heavy)
line: case with the same dependence of K,, on Z,,, but
K = 1.5 cm2 s-l m-l. B. Effect of N recycling efficiency
on mixed-layer concentration of N03; in all cases the
herbivorous microzooplankton excrete N at a rate
equivalent to 40% of their N ingestion rate, and K, is
seasonallv variable as in the lower curve in panel A.
Upper line: high recycling efficiency (q, = 0.6, q2=
0.75); middle (heavy) line: medium recycling efficiency
(q,= 0.5, q2= 0.5); bottom line: low recycling efficiency
(q, = 0.4, q2= 0.25). Numbers to the right of curves
are mean mixed-layer NH, concentrations (mmol N
m -‘) during days 180-280. Data from Fig. 3 -0.
ingested) to be - 65% on average (heavy line
in Fig. 12B). Phytoplankton
stock and NH4
concentration
remain relatively
constant
over the year, so, on average, NO3 uptake
comprised 35% of the total N uptake by the
phytoplankton
and represents a measure of
the extent of preferential utilization of NH,
by the phytoplankton.
Despite the range of predictions,
the
model suggests that a combination
of two
The first presumption is that in the ocean,
as in the model, the entire phytoplankton
assemblage is under grazing control. Takahashi et al. (1990) reported large seasonal
variations of vertical fluxes of diatom fi-ustules in deep sediment trap collections at
Station P. Among the several species sampleld were some very large diatoms (several
tens of micrometers in largest dimension)
such as Chaetoceros atlanticus, Chaetoceros
concavicorne, Corethron criophilum, and
Rhizosolenia alata. The implication of these
flux data is that there are substantial seasonal changes in growth rates and abundance of large diatoms. Although the surface-layer abundances of large diatoms are
indeed highly variable at Station P, the species are always extremely rare, contributing
a very small fraction of the total phytoplankton biomass (Clemons and Miller
1984; Horner and Booth 1990; B. C. Booth
pers. comm.). In contrast, one of these species (C. concavicorne) was the dominant or
codominant species in fall phytoplankton
blooms in coastal Dabob Bay (Puget Sound,
Washington) in 1973,1979,1982,
and 1990
(my unpubl. data). Clearly in Dabob Bay
this large diatom is not controlled by grazing, yet extensive analysis of abundances of
phytoplankton species at Station P show that
neither this species nor any of about a dozen
others has ever reached concentrations remotely approaching those observed during
the blooms in Dabob Bay (Homer and Booth
1990; B. C. Booth pers. comm.).
A possible explanation of the absence of
blooms of large diatoms in open waters of
the subarctic Pacific is that these species are
Grazing in the open sea
limited in their growth by a micronutrient,
perhaps soluble Fe, which is very scarce there
(Martin et al. 1989). Large phytoplankton
species may be more susceptible to Fe limitation (Hudson and Morel 1990). Perhaps
their growth rate is so low that combined
effects of physical losses and sinking dominate their dynamics, and grazing plays a
minor, if any, role in controlling their numbers. For example, previously I (Frost 1987)
suggested that large suspension-feeding copepods (Neocalanus spp.) might be important grazers of large phytoplankton cells, but
abundances of these copepods are at seasonal lows when high autumn diatom fluxes
are recorded (Miller et al. 1984; Miller and
Clemons 1988).
Coastal waters, on the other hand, have
such high concentrations of dissolved Fe that
limitation
of phytoplankton
growth by Fe
is not expected (Martin et al. 1989). The
occurrence of blooms of large diatoms in
coastal waters must then be attributed to
low grazing rates, presumably because microzooplankton are inefficient grazers of the
large cells while meso- and macrozooplankton grazers respond too slowly in their population growth to changes in phytoplankton
abundance (Cushing 19 5 9).
Whether the net specific growth rate of
the phytoplankton
assemblage in the open
subarctic Pacific is lower than expected, given the light and temperature of the mixed
layer, because of scarcity of Fe is a contentious issue (Banse 1990a,b; Martin et al.
1990a). Without getting into the details of
the debate, it seems to me that the lack of
an effect of Fe enrichment on phytoplankton production rate (Martin et al. 1989) is
particularly
crucial negative evidence. It
suggests that the bulk of the indigenous phytoplankton assemblage (i.e. that responsible
for most of the phytoplankton
production)
is not Fe limited in its growth. However,
Martin et al. (1989) did observe an effect of
Fe enrichment on population growth rate
and final yield of phytoplankton
after several days of incubation. Associated change
in species composition of the phytoplankton suggests release from Fe limitation of a
normally rare component that perhaps is
not efficiently grazed by the indigenous
grazer assemblage.
1627
Thus, if we incorporate a possible effect
of Fe deficiency on phytoplankton
species
composition,
surface waters of the open
subarctic Pacific may remain nutrient-replete because of grazing control of phytoplankton stock, coupled with preferential
utilization
of NH4 by the phytoplankton,
yet the grazing control may be exerted on
an assemblage structured by Fe limitation.
A large part of the indigenous phytoplankton assemblage- that responsible for the
bulk of the phytoplankton
production - appears not to be Fe limited. Hence a model
can describe the annual cycle of phytoplankton stock and nutrients quite well without
invoking Fe limitation
of phytoplankton
growth. However, when a natural phytoplankton assemblage is exposed to Fe enrichment, a rare component of the phytoplankton assemblage, normally contributing
little to total phytoplankton
production, is
released from Fe limitation.
This component seems to be large-sized species, chiefly
diatoms (Martin et al. 1989), that cannot be
grazed efficiently by the indigenous grazer
assemblage.
This interpretation
could apply to the
other two nutrient-rich
areas of the open
ocean as well, with a possible additional effect of silica limitation of diatom growth in
the subantarctic circumpolar seas (Sommer
and Stabel 1986). However, the magnitude
of the necessary grazing control would vary
among the nutrient-rich
regions depending
on the actual magnitudes of phytoplankton
net specific growth rates.
The second presumption concerns the fact
that control or regulation of phytoplankton
stock is a property of the entire pelagic ecosystem, not solely a consequence of grazing
(Thingstad and Sakshaug 1990). It is presumed that the grazer trophic guild is insulated from potentially destabilizing predation (Hastings and Powell 199 1; Steele
and Henderson in prep.), otherwise grazer
populations
would occasionally
be depressed by predation and phytoplankton
blooms with attendant nutrient depletion
would occur. Such events would certainly
have been evident, had they occurred, in
the long time-series of observations at Station P, yet there is no record of a phytoplankton bloom of the magnitude of those
1628
Frost
in coastal waters (Fig. 1). Although a model
of an entire pelagic ecosystem is unattainable, the grazing hypothesis implies a pelagic food chain with the following general
hierarchy of control: predators of microzooplankton
predators vood limited) +
predators of microzooplankton
suspensionfeeders (predator limited) + microzooplankton suspension-feeders (food limited)
-+ phytoplankton
(predator limited). That.
is, in order that the hypothesized balance
between phytoplankton growth and grazing
mortality not be disrupted, the predators of
microzooplankton
suspension-feeders must
be kept largely under control by their predators. The composition
of the upper two
trophic guilds in nutrient-rich,
open seas is
unknown, but I have suggested (Frost in
prep.) that in the open subarctic Pacific the
fourth trophic guild must be mesozooplankton-the
size fraction of the zooplankton
dominated by the large Calanoid copepods
Neocalanus spp.
Conclusions
The nutrient-rich
areas of the open sea
are not as biologically
productive as they
might be. Grazing and Fe limitation
have
recently been portrayed as alternative explanations for why phytoplankton stocks are
low and nutrients are underutilized in these
ocean areas. But no single factor can completely explain the pattern, and, like all interesting scientific controversies, the full explication probably will inco.rporate aspects
of both of these hypotheses and perhaps even
others. Surface waters of the Pacific equatorial upwelling zone and the open subarctic
Pacific may remain nutrient-replete because
of grazing control of phytoplankton
stock,
coupled with preferential utilization of NH4
by the phytoplankton.
Yet, the grazing control may be possible only because certain
components of the phytoplankton
assemblage, particularly potentially fast-growing,
inefficiently grazed species, are limited in
their growth by a trace nutrient such as dissolved Fe. The subantarctic circumpolar region may offer the epitome of multifactor
control. Deep mixed layers even in summer
impose greater light limitation
on phytoplankton growth than in the other two nutrient-rich areas. Scarcity of dissolved Fe,
or even Si04, may place an added constraint
on growth of certain components of the phytoplankton, leading to dominance by species, chiefly pica- and nanoplankton-size,
with low requirements for Fe or SiOZ. The
phytoplankton assemblage with low specific
growth rate can, nevertheless, only remain
at 1.0~ concentration
because of grazing
mortality,
probably exerted primarily
by
microzooplankton.
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