JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 2 j PAGES 209–220 j 2006

Modelling of autumn plankton

bloom dynamics
HELEN S. FINDLAY1,2, ANDREW YOOL2*, MARIANNA NODALE3 AND JONATHAN W. PITCHFORD1
1 2
BIOLOGY DEPARTMENT, UNIVERSITY OF YORK, HESLINGTON, YORK YO10 5DD, UK, NATIONAL OCEANOGRAPHY CENTRE, SOUTHAMPTON, EUROPEAN
3
WAY, SOUTHAMPTON SO14 3ZH, UK AND THE MATHEMATICAL INSTITUTE, UNIVERSITY OF OXFORD 24-29 ST GILES’, OXFORD OX1 3LB, UK

*CORRESPONDING AUTHOR: axy@noc.soton.ac.uk

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Received August 15, 2005; accepted in principle October 25, 2005; accepted for publication December 6, 2005; published online December 15, 2005

Communicating editor: K. J. Flynn

A simple system of parametrically forced ordinary differential equations is used to model autumn
phytoplankton blooms in temperate oceans by a mechanism involving deepening of the upper mixed layer.
Blooms are triggered provided the increase in nutrients in the mixed layer is rapid within the first few
days of deepening and provided light-limited phytoplankton growth rate is relatively high. Blooms exist
as transient trajectories between quasi-equilibrium states, rather than as bifurcations of steady states;
therefore very gradual deepening cannot trigger blooms. Very rapid deepening also prevents blooms due to
the deleterious effect on phytoplankton growth rate. The mechanisms identified by this simple model are
vindicated by considering alternative grazing and deepening regimes and by comparison with a more
ecologically complex model (Fasham, 1993, in The Global Carbon Cycle, Springer-Verlag). Modelled
estimates of primary productivity from both the simple model and the complex model parameterized for
Ocean Weather Station ‘India’ are around 0.5 g C m2 day1 during the autumn bloom, therefore
comprising a significant component of annual production in temperate areas.

INTRODUCTION
Phytoplankton populations in most temperate and sub-
polar oceanic regions undergo strong seasonal cycles,
with prominent blooms occurring particularly in the
spring but also to a lesser extent in the autumn.
Understanding the mechanisms causing such blooms,
and quantifying their associated primary production
(and the fate of this primary production), is of fundamen-
tal importance in assessing global carbon budgets and
modelling scenarios of global climate change.
Spring blooms have been studied for many decades
(Sverdrup, 1953; Evans and Parslow, 1985; Lochte et al.,
1993; Truscott, 1995; Bury et al., 2001; Dutkiewicz et al.,
2001), and a good theoretical understanding has been
achieved. It is generally accepted that they are caused by
a combination of vertical stratification of the water column
and increasing solar radiation after the replenishment of
nutrients by convectional mixing over the winter months.
Once initiated, spring blooms are controlled by increasing
zooplankton levels and decreasing nutrient concentration
within the upper mixed layer (Fasham, 1993).
By contrast, autumn blooms are less well studied,
although their occurrence is widely documented
(Raymont, 1963; Hardy, 1970; Ross, 1977; Steele and
Henderson, 1978; Lalli and Parsons, 1997; Herring,
2002). The classic hypothesis suggests that phytoplankton
blooms in autumn are caused by the following mechan-
ism. Increased vertical mixing and the breakdown of
stratification in autumn causes an influx of nutrients
into the upper layers of the ocean. Meanwhile, light
levels remain high enough so as not to limit photosynth-
esis. Grazing by zooplankton will also be affected by
increased vertical mixing—this acts to dilute the grazer
population and may further promote phytoplankton
growth. This combination of factors in principle allows
phytoplankton populations to increase their growth rate
and initiate a bloom. However, this increased vertical
mixing also has negative consequences for phytoplankton
since it mixes them to greater depth and thus decreases
the light levels they experience. Indeed, if phytoplankton
are drawn below Sverdrup’s critical depth (Sverdrup,
1953), then, as a whole, population growth is impossible.

doi: 10.1093/plankt/fbi114, available online at www.plankt.oxfordjournals.org

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 JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 2 j PAGES 209–220 j 2006

Thus, the rate and timing of the breakdown in stratifica-
tion, modelled here as a deepening in the mixed layer, is
predicted to be crucial in controlling the magnitude and
duration of an autumn bloom.
Autumn blooms have been documented in the litera-
ture (Zingone et al., 1995; Edwards et al., 2002; Aiken
et al., 2004), and the seasonal cycles have been quantified
(i.e. phytoplankton concentration and chlorophyll levels
measured), but no mechanism has been analysed with
the important factors being quantified. This investigation
tests the autumn bloom hypothesis by formulating a
simple mixed layer ecosystem model, which is parame-
amount of nutrients (nitrate here), and a lower layer
containing no phytoplankton (because of assumed low
light) but an excess of nutrients, N0 (Evans and
Parslow, 1985).
The model uses three coupled ordinary differential
equations (ODEs) showing the change in mixed layer
depth (MLD) M, nutrient concentration N, and phyto-
plankton concentration P in the upper mixed layer over
time t measured in days (these variables are summarized
in Table I).
dP N m þ hðtÞ

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trically forced by deepening of the upper mixed layer. ¼ rðM ÞP  gP  P ð1Þ
dt kþN M
The mechanisms elucidated in this simple model are
then examined in the context of the more complicated dN N m þ hðtÞ
ecosystem model of Fasham (Fasham, 1993) to determine ¼ rðM ÞP þ ðN0  N Þ ð2Þ
dt kþN M
their general applicability.
dM
¼ hðtÞ ð3Þ
dt

METHODS The model is adapted from the classic model of Evans

and Parslow (Evans and Parslow, 1985), which aimed to
A simple model of the open ocean ecosystem is used model annual plankton cycles and included a fourth
to test the theory of autumn blooms (Fig. 1). The equation describing herbivore dynamics. The herbivore
model is formulated as a bilayer system consisting of equation is here simplified to a constant, g, reflecting
an upper, actively mixed layer (down to the seasonal phytoplankton mortality. If this mortality is assumed to
thermocline) containing phytoplankton and a limited be primarily due to herbivory, then it may be more
appropriate to treat g as a dynamic quantity as described
in detail below. Seasonality in day length is regarded as
negligible over the time scale of an autumn bloom.
Stochastic fluctuations, e.g. in cloud cover, were not
incorporated for the sake of model tractability; this is
Light reasonable in relation to short time scale (hours) fluctua-
tions about a seasonal mean (Truscott, 1995; James et al.,
2003) but may be unrealistic for variability over longer
Uptake time scales (days). In short, equations (1)–(3) represent a
temporal ‘snapshot’ of the annual cycle described by
M Mortality Upper mixed
layer Evans and Parslow (Evans and Parslow, 1985).
loss
Deepening of Evans and Parslow (Evans and Parslow, 1985)
mixed layer describe an asymmetry in the response of the ecosys-
and tem state variables to positive and negative changes in
diffusion the MLD—the simple ecosystem model in this study
focuses solely on the deepening of the mixed layers
Lower
layer over a relatively short, typically 10-day, time period.
N0
Table I: Model state variables
Variable Symbol Unit

Fig. 1. Schematic diagram of the model. Nutrients (N) and phyto- Mixed layer depth M m
plankton (P) are active in the upper mixed layer, which has depth (M);
lower layer nutrients (N0) are introduced into the upper layer by diffu- Nutrient concentration N mmol m3
sion and mixing. Phytoplankton can be lost from the upper mixed layer Phytoplankton concentration P mmol m3
by diffusion and by dilution when the mixed layer is deepening.

210
 H. S. FINDLAY ETAL.
The asymmetry in Evans and Parslow’s study was
generated by the annual variation in deepening and
shallowing of the mixed layer, which is not relevant
here.
Phytoplankton [equation (1)]
Uptake by phytoplankton is modelled with a simple
Michaelis–Menten hyperbola N/(k+N) multiplied by the
light-limited specific growth rate and the phytoplankton
concentration. It is assumed that nutrient is limited by a
saturation maximum and is immediately converted to
growth (i.e. there is no modelling of intracellular pools
of nutrient). Light-limited specific growth rate is a func-
tion of depth, r(M)=a/M (where a is a constant, M is
depth). This approach is taken from Boushaba and
Pascual (Boushaba and Pascual, 2005), who derive this
simplified functional form for photosynthesis within the
mixed layer by implicitly considering irradiance, plank-
ton self-shading and attenuation by water itself. This
functional form is simpler than that used by Fasham
(Fasham, 1993), but the general agreement with simula-
tions using this more complex model (see below) further
justifies its use.
Phytoplankton mortality occurs at a constant per
capita rate, g. This simplifying assumption is used in
other models (Fasham et al., 1990) but is inappropriate
where mortality is dominated by grazing. An alternative
assumption, where a fixed grazer population is able to
remain with the mixed layer, is explored below. Within
the context of this simple model, the parameter g is
chosen so as to produce realistic unforced equilibria for
the (N, P) system; the fact that more complicated models
involving dynamic and nonlinear grazing effects show
the same bloom behaviour as the simple model justifies
this expedient choice.
Phytoplankton concentrations are also affected by
cross-thermocline mixing, m, and by entrainment of
water, h(t), from the lower layer. In both instances,
because it is assumed that there are no phytoplankton
in the lower layer, these processes decrease upper layer
concentrations.
Table II: Model parameters
Parameters Symbol
Deep nutrient N0
Uptake half saturation k mmol m3
Diffusion rate m m day1
Light-limited specific growth rate r (M)
Phytoplankton mortality rate g day1
j MODELLING AUTUMN BLOOMS
Nutrient [equation (2)]
Nutrient concentrations are decreased due to uptake by
phytoplankton, following the Michaelis–Menten rela-
tionship described above. Nutrient addition into the
mixed layer is first modelled as a diffusive process, such
that nutrient concentration in the upper mixed layer,
N, tends toward that in the lower layer, N0, at a rate
(m/M)(N0–N ). Nutrients can also be added to the mixed
layer directly through entrainment due to deepening.
Assuming that the upper layer is always perfectly
mixed, this entrainment occurs at a rate (h(t)/M)(N0–N ).
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Note that phytoplankton losses are not returned as nutri-
ent in this model. They are assumed either to enter
(unmodelled) higher trophic levels, to quickly sink out
of the modelled system as detrital particles, or to be
regenerated in a time frame beyond that simulated.
Forcing [equation (3)]
The dynamic forcing in this model is represented by the
deepening of the mixed layer with deepening rate h(t).
For simplicity, h(t) can be assumed to be constant (y ) for
the 10-day period that the autumn bloom is being simu-
lated. In most simulations presented here, depth is
increased from 25 to 50 m in 10 days, giving a deepening
rate of 2.5 m day1. This is a plausible autumn deepen-
ing regime according to Ryabchenko et al. (Ryabchenko
et al., 1997), who suggest it is these abrupt changes in
MLD that cause the oscillatory phytoplankton behaviour
found in their model and observed data. The effects of
temporally varying deepening regimes, simulating
storms, are described below.
Calculation
Numerical integration of the simple model [equations (1)–
(3)], using an explicit fourth-order Runge–Kutta algo-
rithm with fixed time step (Press et al., 1992), allows a
large range of parameter values to be investigated. Table II
summarizes default parameter values used, based on
those of Evans and Parslow (Evans and Parslow, 1985),
with the implicit phytoplankton mortality parameter
Unit Value Source
mmol m3 10 Evans and Parslow (1985)
0.5 Evans and Parslow (1985)
3 Evans and Parslow (1985)
day1 2 (max) Evans and Parslow (1985)
0.8 This article
211
 JOURNAL OF PLANKTON RESEARCH j VOLUME
calculated so as to produce a realistic equilibrium phyto-
plankton population based on Batten et al. (Batten et al.,
2003) before the deepening of the mixed layer.
Comparison with a seven-component
ecosystem model
The Fasham (Fasham, 1993) plankton ecosystem model
consists of seven state variables linked together to form a
more complete description of the ocean’s nitrogen cycle
than the model used here. Concentrations of phytoplank-
ton, zooplankton, bacteria, detritus, nitrate, ammonium
and dissolved organic nitrogen are simulated by forcing
changes in MLD and light over an annual cycle (for a
given latitude and longitude location). An implementation
of this model by Yool (Yool, 1998) (hereafter referred to as
the YFDM model) was adapted here to reproduce the
MLD deepening used in the simpler two-component
model (i.e. the maximum depth reaches 50 m in winter,
25 m in summer, with shallowing occurring in spring and
deepening occurring in late summer/early autumn).
Phase plane analysis and equilibria of the
simple model
It is useful briefly to consider the model [equations (1)–
(3)] in the absence of the forcing induced by the deepen-
ing of the mixed layer, that is with h(t) set to zero. This
simpler system of two ODEs, modelling nutrient and
phytoplankton dynamics within a mixed layer of con-
stant depth, can be shown to have two physically mean-
ingful equilibria provided
rl> 0
and
lk
N0 > ; bifurcation of steady states, the trajectory of the dynami-
r l
where l = g + d and d = m/M represents the per capita
loss rate for phytoplankton. These criteria are readily
satisfied by the parameter values considered here
(Table II). If they are not satisfied then one is essentially
considering a species or assemblage of phytoplankton
which cannot persist, even at minute levels, in the given
nutrient regime; such situations are not considered here.
One equilibrium is at (N0, 0) and can be shown always to
be a (mathematically unstable) saddle point. The second,
more interesting, equilibrium may be denoted
 
  lk dN0 dk
ðN ; P Þ ¼ ; 
rl l r l
212
28 j NUMBER 2 j PAGES 209–220 j 2006
and this equilibrium can be shown always to be linearly
stable, according to the Routh–Hurwitz criteria or sim-
ple phase plane analysis (Murray, 2002). Thus, in the
absence of forcing, the system will simply equilibrate to
(N *, P *) from any physically realistic initial condition.
Simple algebra reveals that P * decreases as M (depth,
regarded as a fixed parameter) increases but that the
stability of (N *, P *) does not change. At first glance,
this suggests that blooms can never be produced by a
deepening of the mixed layer (i.e. a dynamic increase in
M); as the mixed layer deepens the system is attracted
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towards a smaller equilibrium value of P. This is, how-
ever, misleading; the trajectory followed by the solution
to the system can involve the P population increasing
significantly before settling down to its new equilibrium
value. This will be discussed in more detail, but here it is
sufficient to note that autumn blooms, as described here,
are a purely transient phenomenon; there is no bifurca-
tion of steady states.
RESULTS
The results of simulations using the basic parameter
values (Table II) are shown in Fig. 2a in comparison
with the equilibrium values [the (N *, P *) values of sec-
tion 2.4] calculated at each time step. The system was
allowed to reach its equilibrium value at a constant MLD
of 25 m. The mixed layer was then deepened at a rate of
2.5 m day1, reaching a maximum depth of 50 m after
10 days. In this and subsequent graphs, time in days is
measured from the day on which the mixed layer begins
to deepen. The results show that a phytoplankton bloom
is produced, despite the fact that the equilibrium phyto-
plankton value decreases monotonically during the for-
cing period. This is because, despite there being no
cal system is temporarily attracted towards a quasi-
equilibrium state (Truscott, 1995) with increased phyto-
plankton during the forcing period.
The simulation in Fig. 2b uses the same deepening
regime, but with a different nutrient equilibrium concen-
tration, phytoplankton equilibrium concentration and
mortality constant [(N *, P *, g) = (1, 0.8, 1.2)]. This
illustrates that autumn blooms are not a necessary con-
sequence of the model. Here, under conditions where
phytoplankton mortality is high or nutrients are not
depleted during the summer, the model system will not
show a bloom in response to autumn deepening of the
mixed layer.
A more thorough investigation of parameter space
elucidates which conditions are sufficient to trigger
 H. S. FINDLAY ETAL. j MODELLING AUTUMN BLOOMS

Concentration (mmol N m–3)

Time (days)

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Concentration (mmol N m–3)

Time (days)

b
Concentration (mmol N m–3)

Time (days)
Concentration (mmol N m–3)

Time (days)

Fig. 2. Modelled nutrient, N (top graph—solid line) and phytoplankton, P (bottom graph—solid line) values over a 10-day period of deepening
(deepening rate 2.5 m day1, initial depth 25m) and then a 5-day recovery period (depth maintained at 50m), shown together with equilibrium
values (N*, P*) for nutrient (dots) and phytoplankton (dots) at each depth. Panel a has parameter values taken from Table II, illustrating conditions
sufficient for a bloom [(N*, P*, g) = (0.4, 1.3, 0.8)] and panel b demonstrates parameter values which, under identical forcing, do not trigger a bloom
[(N*, P*, g) = (1, 0.8, 1.2)].

213
 JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 2 j PAGES 209–220 j 2006

autumn blooms. Investigations were carried out for the mortality, phytoplankton more easily escape tem-
main variables, including varying the initial condition porarily onto a bloom trajectory.
(N *, P *), to map out the range of conditions that would (iv) There is an optimum for deepening rate, y, which
cause a temporary bloom in phytoplankton. This then allows a maximum bloom to be produced with
allowed analysis of specific parameters to determine the each set of parameters. As y tends to infinity, the
model’s sensitivity to each. The important results from maximum phytoplankton concentration decreases
this numerical investigation are summarized below and due to the rapid decrease in light-limited specific
in Fig. 3. growth rate and the direct effect of dilution. As y
(i) Increasing N0 enhances the bloom, as might be tends to zero, the phytoplankton population is able
expected because of increased resource availability to follow the equilibrium concentration for each
(e.g. N0 = 10 mmol m3, phytoplankton concen- time step, and no bloom occurs (Fig. 4).
tration increases by 51%; N0 = 20 mmol m3, Primary production can be calculated by integrating

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phytoplankton concentration increases by 65%) the uptake of carbon over the MLD (assuming a fixed
(Fig. 3a). This change is not pro rata since phyto- Redfield C:N ratio, consistent with no nutrient limita-
plankton become more limited by light than nutri- tion). Figure 5 illustrates the primary production pro-
ent availability at larger values at N0. duced from the autumn bloom depicted in Fig. 2—(N *,
(ii) As r(M) is decreased, the magnitude of the bloom is P *, g) = (0.4, 1.3, 0.8) —in comparison to primary
also decreased (Fig. 3b). However, at these lower production produced at the corresponding equilibrium
levels of light-limited specific growth rate, the phy- concentrations and primary production when the growth
toplankton population is sustained at a lower con- rate r(M ) is lowered. Interestingly, when computed over
centration for a longer period. Therefore, when the 10-day deepening period, total primary production is
averaged over the 10-day forcing period, there is found to be quite insensitive to the absolute value of
still a significant increase in phytoplankton concen- phytoplankton growth rate: setting a = 50 m day1
tration above its equilibrium. gives total primary production over the 10 days of 5715
(iii) As Fig. 3c shows, the model is sensitive to changes mg C m2, while a = 20 m day1 gives production of
in the mortality parameter, g. Under decreased 5968 mg C m2. This result arises primarily from the
differing patterns of production across the bloom period,
but also from the initial conditions (N *, P *) going into the
5 a bloom (which are products of the summer equilibrium).
r (M ) = 2
4 Phytoplankton populations in our model with a high
3
r (M ) = 1
growth rate characteristically undergo a rapid increase
2 followed by a rapid decline. In contrast, while
r (M ) = 0.6
1

0
P concentration (mmol m )

0 1 2 3 4 5 6 7 8 9 10
–3

8 b 1.8

6 1.6

4 N0 = 30
1.4
N0 = 20
P concentration (mmol m )
–3

2
N0 = 10 1.2
θ = 10
0
0 1 2 3 4 5 6 7 8 9 10 1
3
c
θ=5
0.8
2 g = 0.5

0.6
g = 0.8
1
θ = 1.25
g=1
0.4
0
0 1 2 3 4 5 6 7 8 9 10
0.2
Time (days)

0
Fig. 3. Phytoplankton concentrations plotted against time with 0 5 10 15 20 25

changes in the following parameters: (a) light-limited specific growth
rate, r(M) (day1); (b) deep layer nutrient concentration, N0 (mmol
m3); (c) mortality parameter, g (day1). Except for the parameter
being varied in each graph, all other parameter values and the deepen-
ing regime are identical to those of the simulations in Fig. 2a.
Time (days)
Fig. 4. Phytoplankton concentrations plotted against time with a
range of deepening rates, y (m. day1). There is an optimum rate
between 2.5 and 5 m day1 that produces the greatest bloom.

214
 H. S. FINDLAY ETAL.
750
700
650
Primary production (mg C m–2)
600
550
500
450
400
350
300
0 1 2 3 4 5 6 7 8 9
Time (days)
Fig. 5. Primary production associated with the bloom of Fig. 2a [(N*,
P*, g) = (0.4, 1.3, 0.8)] (solid line); the bloom where r(M) = 0.8 day1
(instead of 2 day1) (dashed line) and primary production for the
corresponding equilibrium concentrations (dotted line).
populations with a lower growth rate bloom more slowly,
they reach a peak concentration nearly as great but also
decline more slowly. Overall, this more gradual bloom
evolution has similar production, despite phytoplankton
concentrations seemingly experiencing a smaller bloom.
Sensitivity analysis
Alternative grazing functions
The assumption of a constant per capita phytoplankton
mortality rate is not appropriate to situations where
mortality is primarily driven by grazing; an alternative
formulation is more appropriate. Assuming a constant
zooplankton grazer population, ĝ, over the short duration
of a bloom leads to a new equation
dP N ^g P m þ hðtÞ
¼ rðM ÞP   P ð4Þ
dt kþN M M
where ĝ/M parameterizes the reduced concentration of
grazers as the mixed layer deepens [note that, neglecting
diffusion, this is the same process of decreasing concen-
tration due to entrainment from the lower layer as the
final term in the original phytoplankton equation (1)]. It
should be noted that this assumption of constant grazer
population is better suited to meso-, rather than, micro-
zooplankton. The mathematical analysis for this revised
system reveals that again the deepening of the mixed
layer cannot cause any bifurcation of steady states; in
this instance the equilibrium (N*, P*) is invariant to
changes in M. Once more, equilibrium-based analysis
would suggest that deepening of the mixing depth cannot
induce blooms. Figure 6 shows that this is not the case;
j MODELLING AUTUMN BLOOMS
Concentration (mmol N m )
–3
Time (days)
Concentration (mmol N m )
–3
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10
Time (days)
Fig. 6. Modelled nutrient (top graph—solid line) and phytoplankton
(bottom graph—solid line) values with new grazing function (equation
4). Forcing occurs over a 10-day period of deepening (deepening rate
2.5 m day1, initial depth 25m) and then a 5-day recovery period
(depth maintained at 50m), shown together with equilibrium values
(N*, P*) for nutrient (dots) and phytoplankton (dots) at each depth.
with the same deepening rate as in Fig. 2a a phytoplank-
ton bloom is triggered although the equilibrium P and N
values remain unchanged. The general picture is the
same as in Fig. 2. The only major difference lies in the
response of the model to deepening rate y; there is no
intermediate deepening rate associated with maximum
bloom size, rather an increasing deepening rate always
increases bloom size (see Discussion).
Comparison with a seven-component ecosystem model
A potentially serious caveat to the results expressed so far
is that the study makes use of a simple plankton model
that excludes much of the complexity of the ocean eco-
system. For instance, the model includes no grazers and
does not directly consider the remineralization of organic
material. To address this, the behaviour of a model
(Fasham, 1993) that includes many of the processes miss-
ing here is additionally examined.
Simulations were carried out to assess the potential
occurrence of autumn blooms. Using the model’s default
parameters for Ocean Weather Station ‘India’ (located in
the Atlantic Ocean, 598N 198W), a small autumn bloom
can be triggered as soon as the MLD begins to deepen.
The forcing can be controlled to show precisely that it is
this method of MLD entrainment that causes the
increase in upper layer nutrients (Fig. 7). By using a
seasonally constant MLD, the YFDM model supports
the simple model’s demonstration of the importance of
mixing (Fig. 8). In this latter example, while a small
spring bloom is triggered by rising irradiance, the lack
215
 JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 2 j PAGES 209–220 j 2006

Irradiance Irradiance
a a
400 400

(W m–2 )
(W m–2 )

200 200

0 0
Mixed layer depth Mixed layer depth
0 0
b b
–20 –20

(m)
(m)

–40 –40
–60 –60

Phytoplankton (solid) and zooplankton (dashed) Phytoplankton (solid) and zooplankton (dashed)
1 0.3
c c

(mmol m )
(mmol m–3)

–3
0.2
0.5

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0.1

0 0
Nitrate Nitrate
d

(mmol m )
d 0.4

–3
(mmol m )

4
–3

2 0.2

0 0
Primary production (solid) and export (dashed) Primary production (solid) and export (dashed)
0.1
e

(g C m–2 d–1 )
e
(g C m–2 d–1 )

0.6
0.4 0.05
0.2
0
0 0 50 100 150 200 250 300 350
0 50 100 150 200 250 300 350 Time (days)
Time (days)

Fig. 7. YFDM model output showing (a) seasonal PAR; (b) mixed
layer depth (MLD) shallowing from 50 to 25 m then deepening to 50 m
again towards the end of summer. Shallowing and deepening each take
30 days; (c) phytoplankton and zooplankton increase in spring, decline
over summer then bloom again in autumn; (d) the upper layer nutrient
concentration alters with MLD, while the lower layer nutrient concen-
tration remains constant at 10 mmol m3; and (e) primary production
and export are greatest during periods of high phytoplankton concen-
trations. If the deepening rate is increased to 2.5 m day1, the bloom
increases in magnitude to >0.5 mmol m3. Deepening to greater depths
does not increase bloom as long as the rate is the same. Growth rate (Vp)
= 1.3 day1.
of a nutrient pulse in autumn prevents any phytoplank-
ton response.
Further to these baseline simulations, Fig. 9 illustrates
the YFDM model response to parameter manipulations
that approximate to those performed with the two-com-
ponent model. The YFDM model parameters chosen
are: gmax, the maximum specific zooplankton grazing
rate; N0, the subthermocline nitrate concentration; kw,
the attenuation coefficient of seawater; and y, the
autumn deepening rate. In each instance, values of
these parameters either side of the baseline value were
used to explore the response of the model (see the figure
caption for further details).
The model responses closely follow those expected
from the analysis of the two-component model.
Increased zooplankton grazing decreases the autumn
bloom size. Increased subthermocline nitrate increases
the autumn nutrient pulse and increases the bloom size.
Fig. 8. As Fig. 7, but with no change in MLD over the annual cycle.
Increased seawater attenuation [approximating to
decreased r(M)] decreases available light and stunts the
autumn bloom. Furthermore, an increased rate of dee-
pening more rapidly entrains nutrient and increases the
bloom size (although excessive deepening decreases the
bloom through its effect on light availability).
There is an interesting deviation from the expected
results in one instance. In Fig. 9b, increasing N0 results in
a suite of curves with consecutively greater autumn
blooms until the most extreme case, however, where
the bloom is slightly decreased in size. Examination of
this simulation in more detail reveals that, although the
autumnal nutrient pulse fuels production (i.e. the mixed
layer enters the autumn denuded of nutrient), a higher
standing stock of zooplankton (more than double that of
the closest simulation) is able to quickly respond to the
blooming phytoplankton and control their numbers.
The effect of explicit zooplankton grazing has an addi-
tional secondary effect. In Fig. 9a, increasing zooplank-
ton grazing rate decreases the size of the autumn
bloom—in the most extreme simulation, the bloom is
completely absent. Examination of these simulations
finds that, as well as directly preventing the bloom by
grazing down the phytoplankton, the zooplankton also
decrease nutrient consumption during the summer. In
the simulations in Fig. 8a, this means that nutrients are
not depleted during the summer, which decreases the

216
 H. S. FINDLAY ETAL. j MODELLING AUTUMN BLOOMS

Maximum specific grazing rate (g

max
) (interannual and spatial) (Steele, 1958). Breakdown of
3
a vertical stratification at the end of summer is due to the
P (mmol m–3 )

2 predictable decline in solar heating and the less predict-

1
able impact of mixing by weather events or storms. To
examine this, Fig. 10 shows ‘storm’ events simulated
0
Subthermocline nitrate (N ) within the model [equations (1)–(3)] by allowing a sudden
0

b
increase in deepening rate to occur for 1 day, in the
1
P (mmol m–3 )

middle of a slower deepening trend. To enable compar-

0.5
ison, all simulations are constrained to have the mixed
layer deepening from 25 to 50 m over 10 days, with
0 storms of increasing severity occurring on day 5.
Attenuation coefficient (kw)
There is a decrease in bloom size as the magnitude of

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2
c
the storm event increases, due mainly to the sharp
P (mmol m–3 )

1
decrease in light availability with depth, which can
entirely counteract the large increase in nutrient avail-
0
ability caused by the rapid deepening. Simulations of the
Deepening rate (θ ) YFDM model under identical deepening regimes exhibit
1
d similar, although less abrupt, changes in bloom beha-
P (mmol m–3 )

viour (results not shown). These results emphasize the

0.5
0
240 250 260 270 280 290
Time (days)
Fig. 9. YFDM model output showing phytoplankton concentrations
during autumn blooms across ranges of four model parameters: (a)
maximum specific zooplankton grazing rate, gmax; (b) subthermocline
nitrate concentration, N0; (c) attenuation coefficient of seawater, kw; (d)
autumn mixed layer deepening rate, y. In each case, the intermediate
thickness line represents the default value for the parameter, with
progressively thinner lines for lower values (1/2 and 1/4 times baseline
respectively) and progressively thicker lines for high values (two and
four times baseline respectively).
impact of nutrient entrainment during autumn mixing.
These results are analogous to those of Fasham (1995) for
the sub-Arctic Pacific station ‘Papa’. In contrast to the
Atlantic station ‘India’, at this station phytoplankton
concentrations only rarely show a bloom (spring or
autumn) and nutrient concentrations are never limiting.
Zooplankton data and the analysis of Fasham (1995)
suggest that these conditions are caused by zooplankton
control through much of the annual cycle (although the
micronutrient iron is also implicated).
Aside from these interesting deviations, the YFDM
model supports the two-component model’s description
of autumn bloom dynamics.
Variable deepening rates and storms
The previous results all describe the mixed layer increas-
ing in depth at a constant rate. This may be an over-
simplification; it has been argued that introducing a
sudden increase in depth into a gradual deepening in
the autumn, induced by transient storm events, may be
the best way to simulate the observed variability
necessity of including, where possible, a high level of
temporal resolution in models involving the interplay
300 310 320 between physics and biology, particularly where accurate
estimates of primary production are sought.
DISCUSSION
This study shows that autumn blooms can be produced
by the mixing of nutrients into a deepening mixed layer
and reveals the key conditions required to trigger a
bloom; these include surface and deep nutrient concen-
trations, phytoplankton mortality and the rate of mixed
layer deepening.
With these factors in mind, it is useful to explore the
general dynamics of the parametrically forced system
[equations (1)–(3)] to try to understand the conditions
under which autumn blooms are triggered. Examining
the quasi-equilibria to which the system is attracted dur-
ing forcing is helpful. When dP/dt = 0 and dN/dt = 0
with y = 0, forcing does not occur and the system is at
equilibrium (see Fig. 11; the null clines are represented
by dotted lines in this figure). Switching on the forcing
(i.e. setting y to be a positive constant) creates, instanta-
neously, a new N null cline which appears above its
previous location [solid line in Fig. 11]. Whilst the for-
cing persists, the solution trajectory is temporarily
attracted to a quasi-equilibrium value on this new null
cline. When the forcing ceases, the system is attracted to
its new equilibrium (N *, P *) value, at the intersection of
the original (unforced) N null cline and the new P null
cline appropriate to the final MLD. A bloom occurs only
when the attraction towards the quasi-equilibrium state
causes the P population to exceed its original value, as

217
 JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 2 j PAGES 209–220 j 2006

2 –20

1 –40

0 –60
0 2 4 6 8 10 0 2 4 6 8 10
2 –20

Concentration N (dashed), P(solid) (mmol N m )

–3
1 –40

0 –60
0 2 4 6 8 10 0 2 4 6 8 10
2 –20

Depth (m)
1 –40

0 –60

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0 2 4 6 8 10 0 2 4 6 8 10
2 –20

1 –40

0 –60
0 2 4 6 8 10 0 2 4 6 8 10
2 –20

1 –40

0 –60
0 2 4 6 8 10 0 2 4 6 8 10
Time (days) Time (days)

Fig. 10. Phytoplankton and nutrient concentrations over a forcing period with a storm event interrupting the standard deepening event. Storm
events occur in order, from top graph to bottom graph: 0 m day1, 5 m day1, 15 m day1, 20 m day1 and 25 m day1.

10 days (25m)
3
P

2.5

1.5

0.5

0
kl/(r-l)
0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5
N
Forcing on (Forcing off)

Fig. 11. Null clines and example solution trajectory for equations (1)–(3) for (N*, P*) = (0.4, 1.3). Null clines are shown: dP/dt = 0 null cline, solid
line; dN/dt = 0 with y = 0, dotted line; dN/dt = 0 with y = 2.5, solid line. Forcing is turned on at day 0 (25 m) and can either be turned off again on
day 10 (50 m)—thick line or deepening can continue to some extended depth or time (e.g. 200 m—dashed line). In both cases, a bloom is triggered;
the solution trajectory begins at its unforced equilibrium (direction of movement indicated by arrows), but is attracted temporarily towards a quasi-
equilibrium state with increased N and P before returning to its new stable equilibrium value with a higher N but lower P value.

illustrated in Fig. 11. If either N * is too low or P * is too is too small, then although the quasi-equilibrium will be
large, any increase in the nutrients will cause the quasi- above the equilibrium state, the difference between the
equilibrium to be at a lower P level, and hence phyto- two states is only slight and any increase in nutrients will
plankton will always decrease. If N * is close to N0, or P * be unable to stimulate a bloom.

218
 H. S. FINDLAY ETAL. j MODELLING AUTUMN BLOOMS
It is interesting to note the lack of symmetry between
the spring bloom and the autumn bloom. As Figs 7 and 8
illustrate, spring blooms can be driven solely by changes
in the light regime, even in the absence of MLD changes.
By contrast, as Fig. 10 illustrates, autumn bloom devel-
opment is highly dependent on mixing events, and their
evolution is controlled by the decrease of light with both
depth and time. This helps to explain the interannual
variability of autumn blooms by underscoring the impor-
tance of the initial (summer) conditions in addition to the
autumnal mixing conditions. The initial conditions are
intrinsically affected by phytoplankton–zooplankton
dynamics over the spring and summer. A future study,
making use of this simple model and the understanding
of autumn blooms brought about by this paper, might be
to assess the importance of changes in climate, storm
frequency and warming on an annual cycle.
Several coupled atmosphere–ocean models have
shown global warming to be accompanied by an increase
in vertical stratification (Houghton et al., 2001). Such a
change would decrease the rate of vertical mixing in the
ocean, with the primary effect of a reduction in nutrient
mixing into the upper layers. As demonstrated in both
the simple model and the YFDM model, such a decrease
in mixing rate or timing will have a large impact on the
magnitude and period of an autumn bloom. The results
of systematically changing y in the simple model reveal
an optimum rate that produces blooms of greatest mag-
nitude (Fig. 4). Although there is no optimum y in the
YFDM model, it does demonstrate (and echo) the effects
of decreased mixing on primary production.
On a longer time scale, the full effects of global warm-
ing are still unknown. Aside from its local effects on
mixing, ocean warming may also alter the major circula-
tion patterns, which in turn could affect large-scale nutri-
ent distributions (horizontal and vertical). Again,
parameter investigation has shown that any change in
nutrient parameterization (e.g. N0) can affect autumn
blooming. Further, although the major oceanic pathway
for carbon dioxide uptake is through the physicochem-
ical pathway, biological productivity can play an impor-
tant role. In the temperate and subpolar regions to which
the work here is most relevant, Herring (Herring, 2002)
estimates that total primary productivity of between 70
and 120 g C m2 year1. During the autumn blooms
simulated here, the modelled primary production was
approximately 0.5 g C m2, with autumn blooms there-
fore contributing significantly to annual production in
these regions (Fig. 7e). Both models suggest that the
primary effect of global warming will be to decrease the
magnitude of autumn blooms.
The general principles of autumn bloom development
outlined by this modelling study can be applied to ocean
219
datasets to examine their validity. Although in situ sam-
pling may miss autumn blooms because of their relatively
limited duration, synoptic measurements of ocean colour
(e.g. SeaWIFS) and sea surface temperature (as a proxy
for ocean stratification) offer an avenue to test the
hypotheses framed by this study. This will form the
basis of a future paper. The mechanism explored in this
investigation may also be used to explain bloom phe-
nomena in different situations.
In conclusion, the classic mechanism that was long
thought to explain autumn bloom phenomena can be
described by relatively simple equations, which when
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validated with plausible parameters, is a useful tool in
determining the significance of an autumn bloom. The
simple model shows that blooms develop provided that :
(i) The increase in nutrients into the upper layer is
rapid within the first few days of the forcing period,
thus allowing there to be enough nutrients and
light available to trigger a population bloom. This
factor is dependent on the values of the upper and
lower layer nutrient concentrations, the upper
layer becoming depleted of nutrients over the sum-
mer while nutrients remain at relatively high con-
centrations in the lower layer.
(ii) The light-limited specific growth rate is relatively
high, thus allowing phytoplankton growth to re-
establish before becoming drawn to low depths,
and hence low light levels.
(iii) The mixed layer deepens at an appropriate rate.
When the rate is too slow, the change in conditions
for the phytoplankton is not rapid enough to per-
turb them from the steady state. When the rate is
too large, the phytoplankton are moved to depths
with low light levels before they have a chance to
utilize the increased nutrients. (The deepening of
the mixed layer thereby provides the link between
the above two factors.)
More complex models of annual plankton cycles show
the same mechanism at work and can be used in con-
junction with the simple model to assess the impact of
phytoplankton populations on various ecosystem fea-
tures. The contribution of autumn blooms to primary
production can be significant.
ACKNOWLEDGEMENTS
Simple autumn blooms models were initially developed
at a workshop held at the University of California,
Berkeley (ONR Grant ONR_URIP N00014-92-J-1527)
attended by JWP together with Rob Armstrong, John
Brindley, Peter Franks, Hariloas Loukos, Hal Smith and
John Steele. We thank Khalid Boushaba for useful advice
 JOURNAL OF PLANKTON RESEARCH j VOLUME
on phytoplankton growth rates. Andrew Yool is sup-
ported by the UK Natural Environment Research
Council (NERC) on the GENIE project (e-Science the-
matic programme). The authors are grateful to John
Steele, Kevin Flynn and an anonymous referee for their
invaluable comments and suggestions.
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