Journal of Plankton Research Vol.18 no.5 pp.643-657, 1996
The use of sea temperature in characterizing the mesoscale
heterogeneity of phytoplankton in an embayment of the southern
Benguela upwelling system
G.C.Pitcher, A.J.Richardson1 and J.L.Korrubel1
Sea Fisheries Research Institute, Private Bag X2, Rogge Bay 8012 and 'Marine
Biology Research Institute, Zoology Department, University of Cape Town,
Rondebosch, Cape Town, South Africa
Abstract. The role of meteorological events and hydrography in determining changes to the phytoplankton community was investigated in an embayment exposed to a narrow band of coastal upwelling.
Daily sampling demonstrated the importance of advective processes driven by meteorological forcing
in controlling rapid shifts in the biomass and species composition of the phytoplankton community.
Samples of similar phytoplankton composition were associated with different stages of the upwelling
cycle, as defined by an index of biological ageing of upwelled waters. Relationships between the physical, chemical and biologicalfieldswere defined from time-senes measurements. The time elapsed following upwelling, required for the determination of biological rates, was estimated from the rate of
heating. A primary production estimate of 2.14 g C nv2 day^ was derived from determination of the
rate of nutrient depletion, whereas a phytoplankton biomass-nutrient consumption equation provided
an estimate of 3 92 g C m 2 day"'. Both rates were within the range of estimates obtained from in vitro
tracer methods.
Introduction
Upwelling systems are characterized by strong variation in physical processes
which govern nutrient availability and the biological response to nutrient enrichment (Barber and Smith, 1981). Wind-driven upwelling is a feature of ocean circulation along the entire west coast of southern Africa. The topography of the
southern Benguela region is complex, and the coastline is irregular with several
bays and capes. These topographical features shear the wind stress field, giving rise
to alongshore variability with discrete upwelling centres off the Cape Peninsula,
Cape Columbine and Hondeklip Bay (Shannon, 1985). The longshore, equatorward winds responsible for upwelling are determined by the South Atlantic Anticyclone, the pressure field over the adjacent continent and by east-moving
cyclones (Shannon, 1985). Changes in the wind important to the phytoplankton
may be observed on two different scales. First, the South Atlantic Anticyclone,
although maintained throughout the year, undergoes a seasonal shift in position,
migrating southwards during summer and northwards in winter. Combined with
changes in pressure over the African subcontinent, wind-induced upwelling in the
southern Benguela is seasonal, reaching a maximum during spring and summer.
The second modulation of upwelling is provided by wind relaxations or reversals
associated with the passage of cyclones south of the continent during the upwelling
season. As a result of this cyclic weather pattern during summer, upwelling winds
exhibit a periodicity of 5-10 days with reversals of 1-3 days. It is at this scale that
the relationship between meteorological events, hydrography and changes in the
phytoplankton biomass and species composition were investigated in Elands Bay,
© Oxford University Press
643
G.C.Pitdier, AJ.Ridiardson and J.LKorriibel
SEA SURFACE
TEMPERATURE ( "C )
32*30'
17" 30'
Fig. 1. Study area. A montage of upwelling off Cape Columbine and north of St Helena Bay as defined
by aerial radiation thermometry (after Nelson and Hutchings, 1983). Sea temperature was recorded
hourly at 2 m (+) in Elands Bay and a fixed station (*) in 10 m of water was sampled daily.
a small exposed bay situated north of St Helena Bay in an area subjected to a
narrow band of upwelling (Nelson and Hutchings, 1983; Figure 1).
Biologically induced changes in the mesoscale nutrient and oxygenfieldshave in
many instances been used to obtain insight into primary production (Minas and
Codispoti, 1993). These so-called bulk property methods (Platt and Sathyendranath, 1993) require knowledge of the time interval associated with changes to the
chemical field for quantitative interpretation. During the Elands Bay study, biological rates including primary productivity were estimated from changes in sea
temperature, and the mesoscale chemical and biologicalfieldsderived from timeseries measurements. Determination of the rate of heating provided the residence
time or time elapsed following upwelling necessary for these calculations.
Method
Wind observations were made from a meteorological station at Lambert's Bay.
Sea surface temperature was recorded hourly at 2 m in Elands Bay. A fixed station
in 10 m of water was sampled daily for the period 14 February-21 March 1991
(Figure 1). Light-penetration depths were calculated from Secchi disc readings
using an empirical relationship originally proposed by Poole and Atkins (as cited
by Parsons el al., 1977). Temperature profiling of the water column was conducted,
and samples for oxygen, nitrate and chlorophyll a analysis were collected from 0,2,
5 and 9 m. Oxygen concentrations were determined by the Winkler technique.
644
Mesoscale heterogeneity of phytoplankton
Samples for the analysis of nitrate were frozen and later analysed according to the
methods of Mostert (1983). Chlorophyll a samples were analysed by fluorometric
analysis according to Parsons et at. (1984). Samples for phytoplankton analysis
were collected at 0 and 5 m, fixed in buffered formalin and enumerated by the
Utermohl method (Hasle, 1978). Phytoplankton biomass, in terms of carbon, was
estimated indirectly from cell counts and cell volumes (Smayda, 1978). Ciliate
species were also counted and cell volumes converted to carbon assuming
0.1 mg C mnr3 (Banse, 1982). Multidimensional scaling ordination techniques
were used to group samples of similar phytoplankton composition (Field et ai,
1982). Abundance data expressed in terms of carbon were classified using the
Bray-Curtis measure of similarity and summarized in diagrammatic form as an
ordination. Specific growth rates were calculated by means of the equation:
where n, and n2 are phytoplankton biomass measured at time r, and t2, respectively.
Results
Wind and the hydrographic response
The importance of local wind events in determining observed sea surface temperature was clearly evident from continuous wind and temperature recordings for the
period 14 February-21 March 1991 (Figure 2). Sea temperatures were sensitive to
changes in the wind, exhibiting an almost immediate response. Winds with a strong
southerly component (e.g. 14-15 February, 4-6 March) caused water temperatures to decrease as a consequence of upwelling, whereas calmer periods (e.g.
19-24 February, 13-14 March) or periods of northerly winds (e.g. 18-21 March)
caused arisein sea temperature. Superimposed on the synoptic events was a strong
diurnal cycle in the winds. Effects of the diurnal wind pattern and solar heating
were evident at times; sea surface temperaturesrisingduring the day and falling by
as much as 4°C in response to the late afternoon and evening pulsing of the wind
(e.g. 26 February-1 March). Sea surface temperature within the bay therefore
clearly responded to local meteorological forcing with dramatic changes occurring
on scales of hours and days.
The chemical and biological response
Time series
From the time series of wind, temperature, nitrate, oxygen and chlorophyll a, the
possibility of using sea temperature to characterize mesoscale chemical and biological heterogeneity is evident (Figure 3). As already established, periods of
intense southerly wind corresponded to the presence of cold water, whereas
periods of calm or northerly winds were followed by intervals of warmer water
(Figure 3a and b). Nutrient concentrations clearly mirrored sea temperature
645
G.C.Pilcher, AJ.Ricbardson and J.LKornibel
Fig. 2. Wind stick vectors and sea surface temperature recorded for the period 14 February-21 March
1991.
(Figure 3b and c), while oxygen concentrations complemented trends in temperature (Figure 3b and d). As expected, marked changes in chlorophyll a were coincident with changes in sea temperature (Figure 3b and e). The coldest periods of the
study corresponded to periods of very low chlorophyll a, whereas warmer periods
were generally typified by higher concentrations.
Inspection of the vertical distribution of temperature, oxygen, nitrate and
chlorophyll a following selected wind patterns serves to demonstrate both the vertical structure and the extreme temporal variability during the study (Figure 3).
15th February. Strong southerly winds resulted in the presence of a cold (9.310.2°C), well-mixed water column. Low oxygen (0.9-1.8 ml I 1 ), low chlorophyll a
(1.0-2.5 mgnr 3 ) and high nitrate (25.9-27.0 mmol nr3) concentrations were
evident.
24th February. The persistence of calm conditions permitted the development of
vertical structure in the water column. The range in sea temperature (14.0-17.8°C)
and oxygen (2.9-7.8 ml I"1) concentrations was greater and the chlorophyll a maximum (12.1 mg nr 3 ) was now subsurface. Nitrate concentrations were generally
depleted (0-4.0 mmol nr 3 ).
646
Mesoscale heterogeneity of phytoplankton
300
[WIND daily northward displacement (km) |
1tlliir
15 16 17 18 19 20 21 22 23 24 25 26 27 28 1 2
3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
FEBRUARY
MARCH
ffifft
Fig. 3. Time series of (a) wind, (b) temperature, (c) nitrate, (d) oxygen and (e) chlorophyll a
concentrations for the period 14 February-21 March 1991.
9th March. Moderate upwelling winds resulted in cool surface waters (12.4°C) with
high oxygen (5.7 ml I 1 ) and chlorophyll (10.8 mg nr 3 ) concentrations decreasing
with depth. Surface nitrate (5.5 mmol nr 3 ) concentrations were intermediate and
increased with depth.
20th March. Following strong northerly winds the water column, although well
mixed, was very much warmer (13.9-15.0°C) and depleted of nitrate (0 mmol nr 3 ),
while oxygen (5.3-7.9 ml I 1 ) and chlorophyll a (6.2-8.8 mg irr 3 ) concentrations
were elevated.
Light-penetration depths usually varied according to the age of the upwelled
water. The depth of the 1 % light level ranged between 5 and 10 m, with an average
euphotic zone depth of 8.8 m for the period of study.
647
G.C.Pitcher, A J.Richardson and J.L.Korrubel
Biological ageing ofupwelled water
From the time series, it is evident that biologically important elements are mostly
in dissolved inorganic forms in newly upwelled waters and mostly in particulate
organic forms, such as phytoplankton, in aged upwelled water. The ageing status of
a given body of water may therefore be expressed as a relative percentage of these
elements in inorganic and organic forms.
Takahashi et al. (1986) proposed an index of biological aging (IBA) of upwelled
waters:
IB A = 0.59 Chi a/(NO, + 0.59 Chi a)
where the constant 0.59 derived from the chlorophyll a-nitrate relationship was
used to convert mg Chi a to mmol NO3.
Indices were calculated for the present study using chlorophyll a and nitrate data
from 0, 2 and 5 m. In nutrient-rich newly upwelled water, where phytoplankton
concentrations were low, the index tended to zero, whereas in older water, where
chlorophyll a concentrations were high and nutrients low following active phytoplankton uptake, the index tended to one (Figure 4). From the relationship
between the index of biological ageing and temperature, three phases of biological
activity are identifiable in terms of converting inorganic to organic nitrogen: a lowtemperature phase (<11.0°C) where the uptake of nitrate is limited by the small
biomass of a phytoplankton population yet to adapt to conditions of the euphotic
zone; a mid-temperature phase (11.0-14.2°C) where the change in the index of
biological ageing is most rapid; and a high-temperature phase (> 14.2°C) where the
uptake of nitrogen is limited by the depletion of nitrate. The critical temperatures
were derived from the maximum and minimum points of the second derivative of
the fitted equation (Figure 4, inset). Organic forms of nitrogen equalled inorganic
forms at 12.6°C.
Phytoplankton and ciliate species composition
The phytoplankton present during the 36 day time series included members of the
diatoms, the dinoflagellates and a group referred to as the microflagellates. Various species were difficult to identify, and therefore many cells could only be
assigned to genus or higher taxon. Most naked nanoplankton were not readily
identifiable by light microscopy, and were therefore divided on the basis of size and
grouped under the general category of microflagellates.
In excess of 20 diatom species were identified and samples were dominated by
members of the genera Chaetoceros, Nitzschia and Thalassiosira. In all, 11 dinoflagellate species were identified, and the species Prorocentrum micans and Dinophysis acuminata were prominent. Several of the dinoflagellate species were
recognized as heterotrophic. These commonly included species of the genera
Gyrodinium, Polykrikos and Warnowia. The microflagellates were made up of
very small, usually unidentified cells, and in certain instances included rather
larger flagellates, e.g. Eutreptiella species. The ciliate population was dominated
by both oligotrich and tintinnid ciliates. Species of Halteria and Strombidium
648
Mesoscale heterogeneity of pbytoplankton
13
15
TEMPERATURE <°C)
Fig. 4. Regression analysis of the index of biological ageing of upwelled water and sea temperature.
Data from 0.2 and 5 m were best fit by the regression equation: v = e - " ° m i * •""'""VI + e " " ' " ' * w"" 77 '
(r1 = 0.62). Inset: The temperatures delineating three phases of biological activity were derived from
the maximum and minimum points of the second derivative of the fitted equation.
dominated the oligotrich population, while members of the genera Eutintinnus
and Helicostomella were common tintinnid species.
To associate assemblages of phytoplankton with different stages of the upwelling cycle, multidimensional scaling ordination techniques were used to group samples of similar phytoplankton composition (Figure 5). Ordination of the phytoplankton surface samples reflected a graded change in phytoplankton composition
with change in sea temperature. Samples were delineated into the three phases of
biological activity identified by means of the index of biological ageing and sea
temperature, thereby indicating shifts in the phytoplankton composition in response to changes in the hydrological conditions which followed changes in wind
patterns and corresponding advection events.
In examining the different components of the phytoplankton with changes in
temperature, it was evident that various taxa were associated with particular stages
of the upwelling cycle (Figure 6). Changes in microfiagellate carbon (range 1.8129.3; mean 45.7 mg C nr3) concentrations were small relative to those of the diatom (range 2.1-1849.8; mean 598.4 mg C nr3) and dinoflagellate (range 0-3140.7;
mean 449.2 mg C nr3) concentrations. Diatom blooms tended to peak in waters of
intermediate temperature, reflecting their affinity for nutrient-rich waters following upwelling, while dinoflagellate-dominated blooms were found to succeed diatoms and coincided with warm periods following downwelling. The heterotrophic
dinoflagellate biomass (range 0-1021.5; mean 198.3 mg C nr3) contributed on
average 17.1% to the total phytoplankton biomass during the study. The ciliate
biomass (range 0.1-218.0; mean 26.2 mg C nr3) was similar to that of the microflagellate population, with a tendency for higher concentrations in wanner waters.
Ratios of phytoplankton carbon to chlorophyll a varied considerably. It followed, therefore, that chlorophyll a did not accurately reflect phytoplankton
649
G.C.Pitcfier, AJ.Richardson and J.L-Kornjbel
M9 M7
M8
M17 )
F18:
F19
Mil
F17
F14
110
142 C
Fig. 5. Ordination of daily phytoplankton surface samples in two dimensions using multidimensional
scaling for the period 14 February (Fl 4>21 March (M21) 1991. Samples were delineated into groups by
means of sea temperature identified by an index of biological ageing. Axis scales are purely arbitrary.
carbon concentration. The mean ratio for the period of study was 149:1. However,
the ratio in samples with a high dinoflagellate component exceeded 200:1, apparently resulting from the low chlorophyll a content of the dinoflagellate population
(Chan, 1980). Therefore, although the ratio was not uniform, there was a tendency
for it to reflect changes in species composition.
Estimation of biological rates from changes in sea temperature and the mesoscale
chemical and biological fields
The existence of a statistically significant relationship between sea temperature
and an index of biological ageing indicates the potential for estimating the rates
of biological processes, if the residence time of the water can be deduced from
changes in sea temperature. The residence time, or the time elapsed following
the upwelling of water into the surface layer, may be determined by means of
a heat budget.
Calculation of heat gain and time elapsed. The total heatfluxinto the sea surface of
the southern Benguela was determined by Guastella (1992) to be dominated by
incident radiation. Owing to the fact that latent and sensible heat fluxes approximately cancel each other out, the total heat flux can be approximated by the net
radiation: the difference between the total incoming radiation received at the surface and back-radiation from that surface.
650
1O0
IS
3 90
"
11
"
8
IS
8
17
° 0
°
15
IS
15
TEMPERATURE (°C)
13
TEMPERATURE (°C)
13
TEMPERATURE ("O
1}
o
o ° o
o°
"° $ %J^
o
0
17
°
0
(a)
19
0
500
1000
1500
2000
9
3
IS
|
0
60
IX
S 15 °
2500
2S0
•r
4*00
3000
3500
11
13
O
16
B
0
17
0
0
aep°<fla>8o
15
0
TEMPERATURE (°C)
13
TEMPERATURE ft)
13
0 °o° 0
O
0
IS
15
TEMPERATURE (°C)
Fig- 6- (a) Microflagellate. (b) diatom, (c) dinofiagellate and (d) ciliate carbon as a function of sea temperature. Data are from 0 and 5 m.
0 am if .axs<%
9
500
1000
1500
2000
2S00
3000
3500
0
if
<>
°
0
(d)
19
G.C.Pitcher, A J.Richardson and J.L-KomJbel
Guastella (1992) concluded that, for a particular column of seawater, temperature
changes in the mixed layer can be expressed by the relationship:
ATIAt = Qlp^ C p dz
p
where dTis the change in temperature in time At (seconds), Q is the heat input into
the column, pw is the density of seawater (1025 kg nr 3 ), Cp is its heat capacity at
constant pressure (4180 J kg"1 deg~') and dz is the depth (m) of the mixed layer.
The average daily incident radiation during the present study, derived from Cape
Town, was 326 W rrr2 and assuming back-radiation to average 70 W nr2 (Guastella 1992), the net radiation is calculated as 256 W nr2. This heat input is capable
of producing an integrated temperature increase of 0.86°C in the upper 6.0 m
mixed layer over a period of 1 day. The 6.0 m depth reflected the average mixedlayer depth during the period of study, as determined from points of inflection or
transition on the temperature profiles. These profiles reflect combinations of various cases of mechanical wind mixing and thermal mixing, and depended on the
wind strength, insolation and the historical water column characteristics.
Oxygen versus temperature. The influence of biological processes on oxygen concentrations in the upper ocean is well known and oxygen distribution has recently
been used to derive quantitative estimates of biological production (Emerson et
at., 1993). During the period of study, cold upwelling water was typically deficient
of oxygen, whereas high, usually supersaturated oxygen concentrations were
characteristic of warmer water (Figure 7a). The oxygen-deficient water has been
ascribed to both the introduction of water low in oxygen from a remote source and
from local decomposition of planktonic detritus in the water column and at the
sediment interface (Bailey, 1991). Although the relationship between oxygen and
temperature is well defined, calculation of biological production is prevented by
unknown fluxes of air-water gas exchange and transport between the surface and
deeper waters.
Chlorophyll a versus temperature. Chlorophyll a values increased from the low
concentrations evident in cold water to maximum concentrations in waters of
intermediate temperature, before decreasing in yet wanner water in possible
response to the exhaustion of nutrients, increased grazing pressures and a change
in species composition (Figure 7b).
From the regression equation, the chlorophyll a concentration in newly upwelled water of 10°C was estimated to be 1.9 mg nr3, but it increases to a maximum
of 9.1 mg nr 3 at 15.2°C. The time elapsed from upwelling to the bloom peak, based
on the rate of warming of 0.86°C day-', was calculated to be 6.0 days. The specific
rate of observed net growth established from changes in chlorophyll a from the
time of upwelling to the bloom peak was calculated as 0.26 day-1.
Nitrate versus temperature. The inverse relationship between water temperature
and nitrate concentration in the ocean is well established (Kamykowski, 1987).
During the period of study, the curvilinear relationship of the nitrate-temperature
652
9
11
15
13
15
TEMPERATURE <°C)
17
(c)
19
19
0
5
10
15
20
NITRATE (mmd.m 1 )
25
30
35
40
Fig. 7. (a) Oxygen, (b) chlorophyll a and (c) nitrate as a function of temperature and (d) chlorophyll a as a function of nitrate. Data from 0,2 and 5 m were best fit
by the following regression equations: (a) v = 2.905.V - 0.078.V2 - 187652 (F= 103.75. ^ = 0.67, f « 0 . 0 1 ) ; (b) y = e - " J ' M ' " m ' aa*<* (F=23.84, rn = 0.31,
P «0.01): (c) v = (-7.2984 + 121.4537/.r); (F = 76.33. H = 0.66. P « 0 01): (d) y = el""u • a """- Mm"'2 ' '""»»• "• "' (F= 59.59, r3 = 0.79, P «0.01).
10
20
40
13
TEMPERATURE (°C)
(a)
G.C.Pilcber, AJ.Richardson and J.L.Korrubel
data indicates rapid nutrient uptake in relation to the warming of the water, so
depicting the presence of a fast-growing phytoplankton population (Figure 7c).
From the regression equation, it is possible to predict the quantity of nitrate associated with water of a particular temperature. Subsequent determination of the rate
of nutrient depletion by photosynthetic uptake within the euphotic zone provides
an estimate of new production according to the definition of Dugdale and Goering
(1967), which is closely related to export production as formulated by Eppley and
Peterson (1979).
Newly upwelled water of 10°C was calculated to have a nitrate concentration of
23.5 mmol nr3, and at 16.6°C the water was depleted of nitrate. At the rate of
warming of 0.86°C day 1 , nitrate depletion was computed to occur within 7.7 days
at an average consumption of 3.06 mmol NO3 nr 3 day' which equates, via the
Redfield ratio, to the production of 243.3 mg C nr 3 day-' or 2.14 g C nr2 day1.
Chlorophyll a versus nitrate. Chlorophyll a and nitrate concentrations were also
linked (Figure 7d). Chlorophyll a concentrations tended to increase with a
reduction in nitrate, peaking in water low in nitrate before decreasing under conditions of nitrate depletion.
From the regression equation, the maximum chlorophyll a concentration of
12.4 mg nr 3 was observed prior to nitrate depletion at a concentration of
4.6 mmol nr3. It was deduced from the nitrate-temperature regression equation
that the temperature at the time of the bloom peak was 12.9°C. The warming of
water from 10 to 12.9°C at the rate of 0.86°C day 1 would suggest that the bloom
peak was achieved after 3.4 days. The chlorophyll a concentration at the time of
upwelling was inferred from the nitrate concentration of 23.5 mmol nr 3 at 10°C to
be 1.3 mg nv3. Subsequent to upwelling, chlorophyll a concentrations therefore
increased by 11.1 mg nr3, while the nitrate consumption during this period would
have been 18.9 mmol m~3, indicating an average nitrate consumption of
5.6 mmol nr 3 day'. This equates via the Redfield ratio to the production of
445 mg C nr 3 day 1 or 3.92 g C m 2 day ' prior to the bloom peak. The estimated
specific rate of observed net growth, based on changes in chlorophyll a from the
time of upwelling to the bloom peak, was 0.66 day ', and the consumption of
1 mmol NO3 was calculated to yield 0.59 mg Chi a.
Discussion
This 36 day time-series study provided improved information on the events following upwelling, and on the temporal scales and variability of bloom development.
The importance of the advective processes associated with upwelling, and driven
by meteorological forcing, in determining rapid phytoplankton biomass and community changes within the bay was demonstrated. These observations were in contrast to those of a 27 day time-series study conducted in St Helena Bay (Figure 1;
Mitchell-Innes and Walker, 1991; Pitcher etal., 1991), a semi-enclosed system subject to considerably less hydrodynamic variability than that observed in Elands
Bay. During the St Helena Bay study, there was no disruption of the thermocline
and destabilization of the water column as in Elands Bay, where the entire water
654
Mesoscale heterogeneity of phytoplankton
column is replaced during each upwelling event. Biological variability is thus tempered within St Helena Bay and the role of autochthonous phytoplankton species
(Pitcher et al., 1991) and regenerated nutrients (Waldron and Probyn, 1991) in
bloom development and maintenance is enhanced compared to sites of active
upwelling.
Thefindingsof the present study are more comparable to studies conducted in
the discrete upwelling centre off the Cape Peninsula. A set of five drogue studies
conducted in this area provide the most comprehensive attempt to examine
phytoplankton bloom processes subsequent to upwelling (Brown and Hutchings
1987a,b; Brown et al., 1995) in the southern Benguela. The drogue studies found
the cycle of bloom development to be completed within 6-8 days, with a growth
phase of ~3 days. Chlorophyll a concentrations increased from ~1 mg nr 3 in upwelling water to between 10 and 20 mg nr 3 at the peak of the bloom, before
decreasing to concentrations of 1-3 mg nr3. Nitrate concentrations declined from
between 10 and 25 mmol nr 3 following upwelling to 2-3 mmol m~3 at and following the bloom peak. Daily productivity measurements ranged from 0.9 to 7.5, with
a mean of 3.5 g C nr2 day1.
Many of the observations of this study would appear, therefore, to corroborate
the drogue studies. Possibly the greatest discrepancy was the greater magnitude of
the bloom peaks during the drogue studies and the tendency for a greater chlorophyll a yield from nitrate. During the drogue studies, grazing by zooplankton had a
relatively small effect on bloom development (Brown and Hutchings, 1987a).
Although phytoplankton consumption by zooplankton was not estimated during
the present study, grazing by the heterotrophic dinoflagellates and the ciliates may
have contributed significantly to the maintenance of lower than expected phytoplankton biomasses. Heterotrophic dinoflagellates and ciliates occupy different
niches with regard to prey (Hansen, 1991). Despite the greater potential of ciliates
for rapid growth, the considerably higher biomass of the heterotrophic dinoflagellates, and their ability to ingest large phytoplankton species, suggests that their
grazing impact on the phytoplankton population during the present study would
have been greater than that of the ciliates. Minas and Codispoti (1993), using a
similar approach to that of this study, also suggested that herbivore grazing is an
important factor limiting phytoplankton biomass within upwelling systems.
Incident solar radiation provides a major heat source for increasing water temperature coincident with the availability of light for primary production and nutrient uptake, thereby linking temperature, nitrate and chlorophyll a concentrations
(Kamykowski, 1987). Although relationships between chlorophyll a and temperature tend to be poorly defined, as in this study, relationships between nitrate and
temperature have been applied successfully to new production approaches and
modelling (e.g. Dugdale et al., 1989). Because regeneration provides the balance of
the nutrient pool supporting primary production, depletion of a primary nutrient
in order to quantify production will provide an underestimate. However, observed
decreases in the nitrate concentration at the bloom scale during periods of moderate to rapid phytoplankton growth are not thought to be significantly diminished
by regenerated forms of nitrogen. Minas et al. (1986) introduced the term 'net
community production' for productivity estimates derived from nutrient distri655
G.C.Pitcfaer, A J.Richardson and J.I-Korrubel
bution fields. There is, however, general consensus that 'net community production' and 'new production' are similar over phytoplankton bloom time scales
(Platt et ai, 1982; Eppley, 1989). Within Elands Bay, where productivity is driven
mainly by the input of nitrate, estimates of production derived from the rate of
nutrient depletion and by means of a chlorophyll a-nutrient consumption equation are well within the range of estimates obtained from in vitro tracer methods.
Accurate determination of the time elapsed following upwelling is necessary for
the calculation of biological rates by means of bulk property methods. The time
interval determinations of the present study could, in future studies, be improved
by refined heat budget measurements and calculations. Guastella (1992) calculated a rate of heating of 0.65°C day 1 for St Helena Bay for a similar time of the
year. The higher rate of 0.86°C day 1 calculated for this study is anticipated in view
of the shallower environment of Elands Bay. Therefore, although our calculations
lack the sophistication of, for example, the model proposed by Dugdale et al.
(1989), they nevertheless remain a realistic and useful approach to the estimation
of new production under defined conditions.
Acknowledgements
We thank D.Horstman and D.Calder for their role in the field and in the subsequent counting of phytoplankton samples, and J.Taunton-Clark for the provision of sea surface temperature data.
References
Bailey,G.W. (1991) Organic carbonfluxand development of oxygen deficiency on the modern Benguela continental shelf south of 22°S: spatial and temporal variability. In Tyson,R.V. and Parsons.T.H. (eds), Modem and Ancient Continental Shelf Anoxia. Geological Society Special
Publication, No. 58, The Geological Society, London, pp. 171-183.
Banse.K. (1982) Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of
ciliates in the marine pelagial. Limnol. Oceanogr., 27,1059-1071.
Barber.R.T. and Smith.R.L. (1981) Coastal upwelling ecosystems. In Longhurst.A.R. (ed.), Analysis of
Marine Ecosystems. Academic Press, New York, pp. 31-68.
Brown.P.C. and Hutchings.L. (1987a) The development and decline of phytoplankton blooms in the
southern Benguela upwelling system. 1. Drogue movements, hydrography and bloom development.
In Payne,A.I.L., Gulland J.A. and Brink,K.H. (eds), The Benguela and Comparable Ecosystems. S.
Afr. J. Mar. Sci., 5, 357-391.
Brown.P.C. and Hutchings.L. (1987b) The development and decline of phytoplankton blooms in the
southern Benguela upwelling system. 2. Nutrient relationships. In Payne,A.I.L., GullandJ.A. and
Brink JC.H. (eds). The Benguela and Comparable Ecosystems. S. Afr. J. Mar. Sci., 5,393-^*09.
Brown.P.C., Field j.G. and Hutchings.L. (1995) Primary production duringfivephytoplankton blooms
following upwelling. 5. Afr. J. Mar. Sci., in press.
Chan.A.T. (1980) Comparative physiological study of marine diatoms and dinoflagellates in relation to
irradiance and cell size II. Relationship between photosynthesis, growth and carbon/chlorophyll a
ratio. J. Phycol, 16,428-432.
Dugdale.R.C. and GoeringJJ. (1967) Uptake of new and regenerated forms of nitrogen in primary
productivity. LimnoL Oceanogr., 12,196-206.
Dugdale.R.C, Morel,A., Bricaud, A. and Wilkerson J\P. (1989) Modelling new production in upwelling centers: a case study of modelling new production from remotely sensed temperature and color. J.
Geophys. Res.,9*, 18119-18132.
Emerson.S., QuayJ"., Stump.C, Wilbur.D. and Schudlich.R. (1993) Determining primary production
from the mesoscale oxygenfield.ICES Mar. ScL Symp., 197,196-206.
Eppley.R.W. (1989) New Production: history, methods, problems. In Berger.W.H., Smetacek.V.S. and
Wefer.G. (eds). Productivity of the Ocean: Present and Past. John Wiley. New York, pp. 85-97.
656
Mesoscale heterogeneity of pfaytoplankton
Eppley.R.W. and Peterson,B J. (1979) Paniculate organic matterfluxand planktonic new production
in the deep ocean. Nature, 282,677-680.
FieldJ.G., Clarke.K.R. and Warwick,R.M. (1982) A practical strategy for analysing multispecies distribution patterns. Mar. Ecol. Prog. Ser., 8,37-52.
Guastella,L. A.-M. (1992) Sea surface heat exchange at St Helena Bay and implications for the southern
Benguela upwelling system. In PayneA.I.L., BrinkJC.H., Mann.K.H. and Hilborn.R. (eds), Benguela Trophic Functioning. S. Afr. J. Mar. Sd., 12, 61-70.
Hansen.PJ. (1991) Quantitative importance and trophic role of heterotrophic dinoflagellates in a
coastal pelagial food web. Mar. Ecol. Prog. Ser., 73,253-261.
Hasle.G.R. (1978) The inverted-microscope method. In Soumia.A. (ed.), Phytoplankton Manual.
UNESCO, Paris, pp. 88-96.
Kamykowski.D. (1987) A preliminary biophysical model of the relationship between temperature and
plant nutrients in the upper ocean. Deep-Sea Res., 34,1067-1079.
Minas.H J. and Codispoti.L.A. (1993) Estimation of primary production by observation of changes in
the mesoscale nitrate field. ICES Mar. Sd. Symp., 197,215-235.
Minas.HJ., Minas,M. and Packard.T.T. (1986) Productivity in upwelling areas deduced from hydrographic and chemical fields. Limnol. Oceanogr., 31,1182-1206.
Mitchell-Innes.B.A. and Walker.D.R. (1991) Short-term variability during an anchor station study in
the southern Benguela upwelling system: Phytoplankton production and biomass in relation to
species changes. Prog. Oceanogr., 28, 65-89.
Mostert.S.A. (1983) Procedures used in South Africa for the automatic photometric determination of
micronutrients in seawater. 5. Afr. J. Mar. Set., 1,189-198.
Nelson,G. and Hutchings.L. (1983) The Benguela upwelling area. Prog. Oceanogr., 12, 333-356.
Parsons.T.R., Takahashi.M. and Hargave.B. (1977) Biological Oceanographic Processes, 2nd edn. Pergamon, Oxford.
Parsons.T.R., Moita.Y. and Lalli.C.M. (1984)/! Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford.
Pitcher.G.C, Walker.D.R., Mitchell-Innes.B.A. and Moloney.C.L. (1991) Short-term variability during an anchor station study in the southern Benguela upwelling system: Phytoplankton dynamics.
Prog. Oceanogr., 28, 39-64.
Platt.T. and Sathyendranath.S. (1993) Fundamental issues in measurement of primary production.
ICES Mar. ScL Symp., 197,3-8.
Platt.T., Lewis,M. and Geider.R. (1982) Thermodynamics of the pelagic ecosystem: elementary closure
conditions for biological production in the open ocean. In Fasham.M J.R. (ed). Flows of Energy and
Materials in Marine Ecosystems. Theory and Practice. Plenum Press, New York, pp. 49-84.
Shannon,L.V. (1985) The Benguela ecosystem. Part I. Evolution of the Benguela, physical features and
processes. Oceanogr. Mar. Biol. Annu Rev., 23, 105-182.
Smayda.TJ. (1978) From phytoplankters to biomass. In Sournia^A. (ed.), Phytoplankton Manual.
UNESCO, Paris, pp. 273-279.
Takahashi.M., IshizakaJ., Ishimaru.T., Atkinson.L.P., Lee,T.N., Yamaguchi.Y., Fujita.Y. and
Ichimura.S. (1986) Temporal change in nutrient concentrations and phytoplankton biomass in
short time scale local upwelling around the Izu Peninsula, Japan. J. Plankton Res., 8, 1039-1049.
Waldron.H.N. and Probyn,T.A. (1991) Short-term variability during an anchor station study in the
southern Benguela upwelling system: Nitrogen supply to the euphotic zone during a quiescent phase
in the upwelling cycle. Prog. Oceanogr., 28,153-166.
Received on April 25, 1995; accepted on December 4, 1995
657