Hydrobiologia (2005) 540:127–140
Springer 2005
P. Meire & S. van Damme (eds), Ecological Structures and Functions in the Scheldt Estuary: from Past to Future
DOI 10.1007/s10750-004-7128-5
Primary Research Paper
Phytoplankton growth rates in the freshwater tidal reaches of the Schelde
estuary (Belgium) estimated using a simple light-limited primary production
model
Koenraad Muylaert 1,*, Micky Tackx2 & Wim Vyverman1
1
Section Protistology & Aquatic Ecology, Department of Biology, University of Ghent, K.L. Ledeganckstraat 35,
9000 Gent, Belgium
2
Laboratoire d’Ecologie des Hydrosyste`mes, LEH - FRE 2630 UPS-CNRS, Universite´ Paul Sabatier, bât 4R3, 118,
route de Narbonne, 31062 Toulouse Cedex 4, France
(*Author for correspondence: E-mail: [email protected])
Key words: chlorophyll a, freshwater tidal estuary, phytoplankton, production
Abstract
During the course of 1996, phytoplankton was monitored in the turbid, freshwater tidal reaches of the
Schelde estuary. Using a simple light-limited primary production model, phytoplankton growth rates were
estimated to evaluate whether phytoplankton could attain net positive growth rates and whether growth
rates were high enough for a bloom to develop. Two phytoplankton blooms were observed in the freshwater
tidal reaches. The first bloom occurred in March and was mainly situated in the most upstream reaches of the
freshwater tidal zone, suggesting that it was imported from the tributary river Schelde. The second bloom
occurred in July and August. This summer bloom was situated more downstream in the freshwater tidal
reaches and appeared to have developed within the estuary. A comparison between phytoplankton growth
rates estimated using a simple primary production model and flushing rate of the water indicated that no net
increase in phytoplankton biomass was possible in March while phytoplankton could theoretically increase
its biomass by 20% per day during summer. Chlorophyll a concentrations at all times decreased strongly at
salinities between 5–10 psu. This decline was ascribed to a combination of salinity stress and light limitation.
Phytoplankton biomass and estimated annual net production were much higher in the freshwater tidal zone
compared to the brackish reaches of the estuary (salinity > 10 psu) despite mixing depth to euphotic depth
ratio’s being similar. Possible reasons for this high production include high nutrient concentrations, low
zooplankton grazing pressure and import of phytoplankton blooms from the tributary rivers.
Introduction
In estuaries, the influence of the tides usually
extends further inland than the influence of
salinity. As a result, the upper reaches of estuaries
are freshwater systems characterised by the presence of a tidal regime, the freshwater tidal
reaches. Being situated in between the fields of
interest of marine and freshwater scientists, the
freshwater tidal reaches of estuaries have in the
past received relatively little attention. While
several detailed phytoplankton studies have been
carried out in the brackish reaches of the Schelde
estuary (e.g. Van Spaendonk et al., 1993; Soetaert
et al., 1994; Kromkamp & Peene, 1995), little
information is available with respect to phytoplankton in the freshwater tidal reaches of this
estuary.
Estuaries mediate a large part of the nutrient flux
from the land to the sea. As nutrients enter estuaries
through the tributary rivers, concentrations are
often maximal in the freshwater tidal reaches, where
riverine freshwater is not yet diluted by relatively
nutrient-poor seawater. These nutrients provide a
128
high potential for phytoplankton primary production. However, the upper reaches of estuaries,
including the freshwater tidal zone, are often the
location of turbidity maxima. As a result, light
penetration in the water column is low and phytoplankton primary production is often severely lightlimited. This light limitation puts severe constraints
on the development of phytoplankton and prevents
phytoplankton from fully using the available nutrients. Nevertheless, dense phytoplankton blooms
often develop in the freshwater tidal reaches of
estuaries, blooms that have often been found hard
to explain because of the high turbidity of the water
(e.g. Moon & Dunstan, 1990; Cole et al., 1992; Kies,
1997).
In order to reduce the risk of inundations, locks
have been constructed at the freshwater seawater
interface of many European estuaries, thus
reducing most of the freshwater tidal area. In the
Schelde estuary, such locks are positioned relatively far upstream. As a result, the Schelde estuary is one of the few European estuaries that still
possesses extensive freshwater tidal reaches. It
therefore provides a unique opportunity to study
this type of ecosystems in Europe. Previous studies
dealing with phytoplankton in the freshwater tidal
reaches of the Schelde estuary focused on phytoplankton species composition (Muylaert et al.,
1997; Muylaert et al., 2000a) or dealt with the response of summer blooms to short-term variations
in discharge (Muylaert et al., 2001). The goal of
this paper is to document the spatial and temporal
occurrence of phytoplankton blooms in the
freshwater tidal reaches of the Schelde estuary. We
made use of a simple light-limited primary production model to evaluate whether these phytoplankton blooms could have developed in situ.
Materials and methods
Study site
The Schelde estuary is a coastal plain estuary situated in Belgium and The Netherlands (Fig. 1).
Due to high anthropogenic inputs, nitrogen and
phosphate concentrations are very high, especially
in the freshwater tidal reaches. Freshwater discharge is low compared to the total volume of the
estuary and as a result residence time of the water is
long and the salinity gradient is gradual. Residence
time for the entire estuary is about 75 days (Heip,
1988) and salinity increases slowly from 0.5 to
20 psu over a distance of 60 km. The freshwater
tidal reaches of the Schelde estuary include two
major basins, the Schelde and the Rupel basin.
Figure 1. Map of the Schelde estuary showing the location of the sampling stations (black dots) and their distance to the mouth of the
estuary. The upper limit of tidal influence is indicated with grey arrows.
129
This study focuses on the longest of the two basins,
the Schelde basin. The freshwater tidal reaches in
this basin range from Temse to Gent, extending
over a distance of about 60 km (Meire et al., 1994).
Sampling and analyses
For this study, 12 sites situated along a longitudinal transect in the upper reaches of the Schelde
estuary were sampled monthly during the course
of 1996. The 7 most upstream stations of this
transect were situated in the freshwater tidal
reaches while the downstream stations covered
part of the salinity gradient. Subsurface samples
were taken from a ship using a Niskin sampler or
by means of bucket hauls if currents were too
strong. For chlorophyll a analysis, 100 ml water
was filtered over a Whatmann GF/F filter which
was stored at )20 C. Chlorophyll a was extracted
in 90% acetone and quantified using high pressure
liquid chromatography (Wright et al., 1991). Suspended particulate matter (SPM) concentration
was determined gravimetrically after filtration of
subsamples on preweighed GF/F filters. Salinity
and temperature data (measured in situ using a
Datasonde 3 Multiprobe logger) were kindly
provided by Stefan Van Damme.
Assessment of the volume of the estuary
In order to estimate the flushing rate of the water in
the freshwater tidal reaches, the volume of this part
of the estuary needed to be estimated. Therefore,
the freshwater tidal reaches of the Schelde estuary
were divided into equal compartments, one compartment for each sampling station. For about 20
evenly distributed locations in each compartment,
width of the estuarine channel at 1 m depth intervals was measured on bathymetrical maps. For
each compartment, the average width for 1 m
depth intervals was then calculated and a third
order polynomial regression was fitted to the relation between basin width and depth. Cross surface
area was calculated by integrating the resulting
equation between depth at mid-tide and maximum
depth. The average volume of each compartment
was then calculated by multiplying length and cross
surface area. According to these calculations, the
total volume of the freshwater tidal reaches in the
Schelde basin was estimated to be 49 · 106 m3.
Primary production modelling
A modelling approach was adopted to evaluate
whether phytoplankton can attain net positive
growth rates in the freshwater tidal reaches of
the Schelde estuary and whether growth rates are
sufficiently high for phytoplankton blooms to
develop in this part of the estuary. In estuaries,
nutrients and light are generally the major
factors that regulate primary production
(Underwood & Kromkamp, 1999). In the freshwater tidal Schelde estuary, nutrients are probably not important regulators of primary
production. Dissolved inorganic N and P levels
never decrease to concentrations below respectively 240 lM and 5 lM (unpublished data,
Stefan Van Damme). Si is an essential nutrient
for diatoms, the dominant algal group in the
estuary (Muylaert et al., 2000a). Si concentrations sometimes decrease to potentially limiting
levels in summer but Si regulates primary production only during short periods when phytoplankton biomass is maximal (Muylaert et al.,
2001). Therefore, like in many macrotidal estuaries (Monbet, 1992) light is probably the dominant factor limiting primary production in the
freshwater tidal reaches of the Schelde estuary.
In ecosystems where light is limiting phytoplankton growth, primary production can often be
accurately estimated using a modelling approach
(Pennock, 1985; Cole & Cloern, 1987; Cole, 1989;
Grobbelaar, 1990). Therefore, we used a simple
light-limited primary production model to estimate phytoplankton growth rates in the freshwater
tidal reaches of the Schelde estuary. In our model,
real data on chlorophyll a concentration, temperature, irradiance, turbidity and water column
depth were combined with published parameters
of phytoplankton physiology to estimate net primary production in the estuary. An overview of
the variables and parameters used in this model
together with their associated assumptions
and approximations is given in Table 1. In the
model, depth-integrated or areal gross primary
production (Pg,a, in mg C m)2 day)1) was calculated for each station situated in the freshwater
tidal reaches (7 stations situated upstream of
94 km) and for each sampling occasion according
to a formulation that was adapted from Behrenfeld
& Falkowski (1997):
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Table 1. Overview of the variables and parameters used in the model with comments on the assumptions and approximations used
Abbreviation
Units
Variable/parameter
)3
Comments
chla
mg m
chlorophyll a concentration
Measured in situ.
P*m
mg C
maximum specific
Estimated to be 5 at 10 C. This estimate is based on
(mg chl a))1h)1
photosynthetic rate
estuarine primary production studies (Joint & Pomroy,
1981; Malone & Neale, 1981; Cole et al., 1992; Van
Spaendonk et al., 1993) and falls within the range of
measurements carried out in the Schelde estuary
(Jean-Pierre Vanderborght, unpublished results). Pm
was assumed to increase with temperature, having a Q10
of 2.3 as has been observed in estuaries by Joint &
Pomroy (1981) and Malone (1977).
DL
h
daylength
Calculated from date and latitudinal position.
Kd
m)1
extinction coefficient
for downward
Estimated from SPM concentration using a conversion
factor of 0.06 m)1 (mg l)1))1 based on estuarine data
irradiance
(Cloern, 1987).
SPM
mg l)1
suspended particulate
Measured in situ. Concentrations varied considerably
matter concentration
between sampling dates probably because SPM fluctuates strongly during each tidal cycle and because
samples were not always collected during the same
phase of the tidal cycle. Therefore, we used an annual
Eavg
lEinst m)2 s)1
average daily
average SPM concentration for each sampling station.
Data measured near Brussels by the Belgian Royal
irradiance
Meteorological Institute. To smooth out stochastic day-
at the water surface
to-day fluctuations in irradiance, mean Eavg of the week
preceding the sampling campaign was used.
a*
mg C (mg chl a))1 h)1
maximum light
Estimated to be 0.05. This estimate is based on estuarine
[lEinst m)2 s)1])1
utilization
primary production studies (see Pm ).
coefficient
Ra
mg C m)2 day)1
daily areal activity
respiration
Rm
mg C m)2 day)1
daily areal
Estimated to be 5% of Ba respired daily at 10 C.
maintenance
Maintainance respiration was assumed to increase with
Estimated to be 25% of Pg,a. Accounts for the loss of
fixed carbon due to biosynthesis of new biomass
(Raven, 1984).
respiration
temperature, having a Q10 of 1.4 (Tang & Peters, 1995).
Represents the energetic cost of the basal metabolism.
Ba
mg C m)2
areal biomass
Estimated from the water column depth at mid-tide and
chlorophyll a concentration using a C to chlorophyll a
ratio of 30. This ratio is based on a regression of
chlorophyll a concentration against phytoplankton
biomass estimated from cell counts and biovolume
measurements (Muylaert et al., 2001).
V
m3
volume of the section
The volume at mid-tide was used in the calculations.
of the estuary modelled
Q
m3 day)1
total daily discharge
Data provided by the Belgian Waterways and Maritime
of the
section of the estuary
Affairs Administration. To smooth out stochastic
variations in discharge, mean Q of the week preceding
modelled
the sampling campaign was used.
131
Pg;a ¼
chla Pm DL
Kd
ln Eavg a Pm þ 0:82 :
In the original equation of Behrenfeld and
Falkowski (1997), we replaced Popt (the maximum
specific photosynthetic rate as measured under
conditions of variable irradiance) with Pm and we
replaced Ek (the light saturation parameter) with
Pm =a .
In turbid estuaries phytoplankton often spends
more time in darkness than in the light and
therefore respiration strongly influences phytoplankton growth rates. Therefore, Pg,a was
corrected for respiration to yield areal net primary
production (Pn,a, in mg C m)2 day)1). In the
calculation of Pn,a, a distinction was made between
activity and maintenance respiration: Pn;a ¼ Pg;a Ra Rm . The separation of activity and maintenance respiration corresponds more closely to
observations in physiological studies then the more
frequently used approach where respiration is assumed to be a fixed fraction of Pm (Weger et al.,
1989). Moreover, Kromkamp & Peene (1995)
demonstrated that in highly turbid estuaries this
two-compartment respiration model is essential to
obtain positive net primary production rates.
Phytoplankton growth rates (in day)1), not
taking into account any losses other than respiration, were calculated for each sampling
point in
space and time as l ¼ ln Ba þ Pn;a Ba . Phytoplankton blooms can develop only when growth
rates are higher than the flushing rate of the
water. Therefore, for each month, flushing rate of
the water in the freshwater tidal reaches was
compared with the average growth rate of the
phytoplankton in the freshwater tidal reaches. In
the calculation of the average growth rate, growth
rates for each section were weighted by the volume of that section. Flushing rate of the water in
the freshwater tidal reaches was calculated as
lnðV Q=V Þ.
Results
Spatial variation of some important parameters in
the upper Schelde estuary is shown in Fig. 2.
Salinity was below 0.5 psu throughout the year at
the 6 most upstream stations sampled
(111–155 km) and was on average only 0.6 psu at
94 km. These 7 most upstream stations, which are
situated upstream of the confluence of the Rupel
and Schelde basins, were considered to comprise
the freshwater tidal reaches. From 85 km downstream, salinity increased rapidly to an annual
average of 11.5 psu at the most downstream station sampled. Suspended matter concentrations
displayed large variability between the sampling
occasions. The highest annual average concentration was observed in the freshwater tidal reaches at
122 km. A second, smaller maximum occurred in
the salinity gradient around 72 km. Average depth
increased from only 2.4 m near Gent to about 7 m
at 85 km and varied between 7 and 10 m at the
stations downstream from km 85. Average cross
surface area gives an idea of the increase in volume
per unit distance. Cross surface area increased
exponentially in downstream direction. Euphotic
depth (Ze) was calculated as 4.61/Kd (Kirk, 1994)
with Kd being estimated from SPM concentrations
(see Table 1). Mixing depth (Zm) to euphotic
depth ratio’s were low (minimum 1.6) in the uppermost stations sampled. Due to an increase in
both average depth and SPM concentrations, the
mixing depth to euphotic depth ratio increased
rapidly to about 10 downstream from 120 km.
Figure 3 illustrates temporal variations in discharge, irradiance and temperature. Discharge of
the Schelde estuary in 1996 was low compared to
previous and following years. Discharge was relatively constant throughout most of the year,
with irregular discharge peaks in February and
August and an overall increase in November and
December. Average river discharge for the week
preceding each sampling campaign displayed the
same seasonal trend. In September and December
when discharge was maximal, the tributaries of the
Schelde and the Rupel basin contributed equally to
the total discharge of the estuary. When discharge is
low, water from the Schelde river is diverted from
the estuary towards the canal linking Gent directly
with the Westerschelde. Therefore, when discharge
was low, the tributaries from the Rupel basin contributed more (up to 77% in July) to the total discharge of the estuary than the Schelde basin
tributaries. Due to a maximum in day length and
solar inclination, total daily irradiance was highest
in June. Despite large day-to-day variability, average total daily irradiance of the week preceding each
132
sampling campaign displayed the same seasonal
trend. Temperature lagged behind on irradiance
and was maximal in August. Some spatial variation
in temperature was usually observed, with warmer
water temperatures in the most upstream stations in
winter and vice versa in summer.
Figure 2. Spatial variation of some abiotic variables in the upper reaches of the Schelde estuary: salinity (a), suspended particulate
matter (b), cross surface area (c), tidal range (broken lines) and mixing depth (solid line) (d) and mixing depth to euphotic depth ratio
or Zm/Ze (e). Depth and mean water level at high (AHT) and low tide (ALT) are expressed with respect to average low tide water level
at Antwerp. For salinity and SPM, annual mean levels (solid points) and twice the standard deviation (error bars) are presented for
each station.
133
Figure 3. Temporal variation of river discharge (a), irradiance (b) and water temperature (c). Day-to-day variation in discharge of the
Schelde estuary at the confluence of the Schelde and Rupel subbasins is presented as a solid line. Average discharge of the week
preceding the monthly sampling campaigns for the Schelde, Dender and Rupel rivers is indicated in the stacked bars. Day-to-day
variation in irradiance is represented as a solid line while average irradiance of the week preceding the sampling campaign is indicated
as solid points connected by a broken line. Average water temperature (solid points connected by a broken line) and 2· the standard
deviation (error bars) for all sampled stations are given for each month.
Chlorophyll a concentrations at all times
decreased towards the most downstream situated, brackish stations (Fig. 4). In January and
February, chlorophyll a concentrations were low
(<20 lg l)1). A first phytoplankton bloom
occurred in March when chlorophyll a concentrations exceeded 60 lg l)1. During this bloom, highest
chlorophyll a concentrations were observed in the
most upstream stations sampled. Chlorophyll a
concentrations were lower in April and May and
increased again in June. In July and August a second
bloom occurred, with chlorophyll a concentrations
exceeding 50 lg l)1. During this bloom, phytoplankton biomass was maximal in the most downstream situated stations of the freshwater tidal
reaches and decreased not only in downstream
direction but also towards the head of the estuary.
From September onwards, chlorophyll a concentrations decreased again to levels below 20 lg l)1 in
most stations and attained a minimum in December.
Phytoplankton growth rates estimated using
our primary production model at all times differed
134
80
January
May
September
February
June
October
March
July
November
April
August
December
µg chl a l-1
60
40
20
0
80
µg chl a l-1
60
40
20
0
µg chl a l-1
80
60
40
20
0
µg chl a l-1
80
60
40
20
0
40
60
80
100
120
140
160 40
60
80
Km
100
120
Km
140
160
40
60
80
100
120
140
160
Km
Figure 4. Spatial and temporal variation in chlorophyll a concentration in the upper reaches of the Schelde estuary.
strongly between the upper and lower stations of
the freshwater tidal reaches. Annual average
growth rate was highest in the most upstream
station of the freshwater tidal reaches and
decreased rapidly in downstream direction to an
average rate of less than 0.1 day)1 at 122 km and
remained more or less constant at the more
downstream situated stations of the freshwater
tidal zone (Fig. 5). Phytoplankton growth rates
were highest in summer and lowest in winter.
Average growth rate for the entire freshwater tidal
reaches weighted by the volume of each compart-
ment varied between negative rates in January and
December to a maximum of 0.23 day)1 in June
(Fig. 6). Flushing rate of the water in the freshwater tidal reaches averaged over the year
was 0.05 day)1 and, logically, displayed the same
seasonal trend as discharge. Flushing rate displayed a peak in September and in December.
Between January and March and in September,
November and December, average growth rate of
phytoplankton in the freshwater tidal reaches was
lower than the flushing rate of the water. Between
June and August the largest difference between
135
Figure 5. Annual net production and respiration and annual average phytoplankton growth rates at the sampling sites situated in the
freshwater tidal reaches. Production, respiration and growth rates were estimated using a light-limited primary production model (see
text).
average growth rate and flushing rate was observed. Annual areal net primary production and
respiration for each sampling station were estimated by adding up daily primary production and
respiration rates for all months and multiplying by
30.5 for the average number of days in each month
(Fig. 5). Annual respiration and annual net primary production rates did not vary systematically
among the sampling stations. Estimated annual
net production varied between 108 and 294 mg C
m)2 year)1. Estimated annual respiration was high
at all stations and ranged between 30 and 56% of
annual gross production.
Discussion
In the freshwater tidal reaches of the Schelde
estuary, two phytoplankton blooms were observed
0,25
0,20
growth rate
flushing rate
day-1
0,15
0,10
0,05
0,00
-0,05
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
Month
Figure 6. Annual variation in average phytoplankton growth rate and flushing rate of the water in the freshwater tidal reaches. In the
calculation of the average growth rate, the growth rate of each compartment was weighted by the volume of that compartment.
Phytoplankton growth rates were estimated using a light-limited primary production model (see text).
136
in 1996: a spring bloom that occurred in March
and a summer bloom that occurred in July and
August. During the spring bloom in March, irradiance and temperature were low. Phytoplankton
growth rates estimated using our primary production model were accordingly low, on average
only 0.05 day)1 for the entire freshwater tidal
reaches. At that time, river discharge was relatively
high and the flushing rate of the freshwater tidal
reaches calculated for that month was slightly
higher than the average growth rate. This means
that in March, given the environmental conditions
prevailing in the estuary and assuming a normal
phytoplankton physiology, losses due to downstream displacement of water probably exceeded
growth of phytoplankton within the estuary. In
March, highest chlorophyll a concentrations were
observed in the most upstream stations of the
freshwater tidal reaches, where the river Schelde
enters the estuary. This suggests that the phytoplankton bloom observed in March was imported
from the river Schelde. Chlorophyll a concentrations did not increase in downstream direction,
which supports our hypothesis that at that time no
net growth was possible within the estuary.
During summer, chlorophyll a concentration
peaked in July and August, with a maximum of
55 lg l)1 in August. The onset of this summer
bloom, however, could already be observed in
June, although chlorophyll a concentrations at
that time remained below 25 lg l)1. During this
summer bloom, irradiance and temperature were
high and estimated average phytoplankton growth
rate for the freshwater tidal reaches was 3 to 4
times higher than in March. Simultaneously, discharge of the estuary had slightly decreased,
resulting in a large difference between growth rate
and flushing rate. According to our calculations,
the difference between phytoplankton growth rate
and the flushing rate of the water would allow
phytoplankton to increase its biomass in the
estuary by about 20% each day, which is sufficient
to form a bloom. During the summer bloom,
chlorophyll a concentrations were maximal in the
most downstream stations of the freshwater tidal
reaches and in the oligohaline zone while chlorophyll a concentration was lower in the most upstream stations, where the river enters the estuary.
This suggests that the summer bloom, in contrast
to the spring bloom, was not imported from the
river but had developed within the estuary. This
was also confirmed by observations on phytoplankton species composition. While during the
spring bloom, species composition in the estuary
was the same as in the river, during summer, a
different community was observed in the river and
in the estuary (Muylaert et al., 2000a). During the
summer bloom, the chlorophyll a maximum was
situated close to the confluence of the Rupel and
the Schelde. Given the high discharge of the Rupel
basin compared to the Schelde basin this might
suggest that the phytoplankton bloom occurring in
the Schelde basin was imported from the Rupel
basin. Chlorophyll a concentration in the Rupel
basin, however, was less than 10% higher than in
the Schelde basin in June and July and was even
slightly lower than in the Schelde in August.
Moreover, upstream transport of a phytoplankton
bloom from the confluence of the two basins into
the Schelde basin by means of tidal mixing is unlikely to be important as the brackish water (about
2 psu) occurring near the confluence is not transported significantly upstream in the Schelde basin.
Chlorophyll a concentrations observed in the
freshwater tidal reaches were relatively high compared to those observed in the brackish reaches of
the Schelde estuary, the Westerschelde. In the
Westerschelde, at salinities above 10 psu, chlorophyll a concentrations are usually below 20 lg l)1
(Van Spaendonk et al., 1994). During another
study carried out in 1996, chlorophyll a concentrations in the freshwater tidal reaches of the
Schelde estuary exceeded 100 lg l)1 (Muylaert
et al., 2001). In other years, chlorophyll a
concentrations exceeding 200 lg l)1 have been
observed (Van Spaendonk et al., 1993; Lionard
et al., 2005). In turbid estuaries like the Schelde
estuary, phytoplankton primary production is
mainly regulated by concentrations of suspended
matter (Cole & Cloern, 1987; Cole et al., 1992;
Monbet, 1992; Kromkamp & Peene, 1995; Kocum
et al., 2002). In the Schelde estuary, highest suspended matter concentrations were observed in the
upper reaches of the estuary with a peak in the
freshwater tidal zone. The occurrence of a turbidity maximum in the freshwater tidal reaches
can probably be ascribed to the process of ‘tidal
pumping’ or the repeated resuspension and sedimentation of suspended matter in an asymmetric
tidal cycle (Wolanski, 1995; Salomons et al.,
137
1988). In the freshwater tidal reaches, sediments
are brought into suspension when flood and ebb
currents are strongest and partly settle out of the
water column during slack tides. Due to the funnel-shape of estuaries, flood currents are stronger
than ebb currents in the upper estuary. As a result,
more sediment is brought in suspension during
flood than during ebb tide. This results in a net
upstream transport of suspended matter and the
formation of a turbidity maximum. Because suspended matter concentrations are maximal in the
freshwater tidal reaches, it is unexpected to find
highest chlorophyll a concentrations in this part of
the Schelde estuary. Growth of phytoplankton,
however, is determined by the ratio of carbon
fixation and respiration. While carbon fixation
occurs only in the light, respiration takes place in
the light as well as in the dark. The mixing depth
to euphotic depth ratio (Zm/Ze) is an indicator of
the time spent by phytoplankton in the dark relative to the time spent in the light. Although suspended matter concentrations in the Schelde
estuary are maximal in the freshwater tidal
reaches, water depth in this part of the estuary is
relatively low. As a result, the Zm/Ze ratio is in the
freshwater tidal reaches is similar to the Zm/Ze
ratio in the brackish reaches of the estuary and
light limitation should therefore be comparable.
Despite the high suspended matter concentrations,
dense phytoplankton blooms can develop in the
turbid freshwater tidal reaches of the Schelde
estuary thanks to the relatively shallow depth of
the water column.
Chlorophyll a concentrations at all times
declined going from the freshwater tidal reaches
towards the salinity gradient. While chlorophyll a
concentration continued to increase in the oligohaline zone (up to 5 psu), a steep decline was
observed in the mesohaline zone (between 5 and
10 psu), where chlorophyll a concentrations were
always below 10 lg l)1. This decline has also been
reported in previous studies in the Schelde estuary
(Van Spaendonk et al., 1993; Muylaert & Sabbe,
1999). A decline in phytoplankton biomass at the
freshwater seawater interface is typical for many
estuaries and is often ascribed to osmotic stress
(e.g. Kies, 1997). In experiments with phytoplankton communities from the Schelde estuary
where salinity was manipulated, however, salinity
stress alone could not explain the decline in phy-
toplankton biomass at the salinity gradient
(Lionard et al., 2005). In this part of the estuary,
suspended sediment concentrations were similar to
those in the freshwater tidal reaches. High suspended matter concentrations in this part of the
estuary are associated with a weak salinity stratification in the water column and are probably
maintained by trapping of particles in the residual
salt wedge circulation (Wollast, 1989). As water
depth is higher when compared to the freshwater
tidal reaches, the Zm/Ze ratio is also higher and
therefore, phytoplankton is probably more lightlimited at the freshwater seawater interface when
compared to the freshwater tidal reaches. Therefore, light limitation may be equally important for
the decline of phytoplankton biomass in this part
of the estuary as osmotic stress.
The production model used in this study is only
a simplification of the complex processes that affect primary production in the freshwater tidal
reaches. The parameters describing productivity
and respiration used in the model were not determined in situ but were taken from the literature.
While some parameters like Pm and a* can readily
be measured, however, parameters describing
phytoplankton respiration are almost impossible
to measure in the field. In the model, an annual
average value of SPM concentration was used for
each station while SPM concentrations vary
strongly at time-scales ranging from the semidiurnal tidal cycle over the spring-neap tidal cycle to
seasonal variation related to river runoff. The
interaction between variations in suspended matter
concentrations during the tidal cycle with changes
in surface irradiance throughout the day may
cause significant day-to-day variations in productivity (Desmit et al., unpublished results). In the
model, an average value for water column depth
was used while depth varies strongly throughout
one tidal cycle. Despite these shortcomings, we
nevertheless think that our model yields estimates
of annual net primary production that are within
the right order of magnitude. Annual rates of net
primary production for the freshwater tidal
reaches of the Schelde estuary estimated using this
model varied between 108 and 294 g C m)2 year)1.
Despite annual average growth rates being much
higher in the most upstream situated stations,
annual net primary production was not higher in
the upper compared to the lower stations of the
138
freshwater tidal reaches. This can probably be
ascribed to the fact that biomass was much higher
during the most productive season in the lower
stations, resulting in a high production despite low
growth rates.
Average net production for the entire freshwater tidal reaches weighted by the surface of each
compartment amounted to 181 g C m)2 year)1.
This is much higher than annual net production
estimated using a primary production model in the
Westerschelde (41 g C m)2 year)1, Soetaert et al.,
1994). This contrasts with the accepted theory that
in estuaries, primary production increases in seaward direction due to a decrease in turbidity (Heip
et al., 1995). Phytoplankton can attain a higher
annual net primary production in the freshwater
tidal reaches than in the brackish reaches of the
estuary despite Zm/Ze ratio’s being similar because
phytoplankton attains a higher biomass in the
freshwater tidal reaches. High phytoplankton
biomass has been observed in the freshwater tidal
reaches of many other estuaries of temperate
regions in Europe, North America or Asia (e.g.
Sellner et al., 1988; Moon & Dunstan, 1990;
Schuchardt & Schirmer, 1991; Cole et al., 1992;
Murakami et al., 1992). With respect to the
Schelde estuary, several reasons can be put forward for these high chlorophyll a concentrations.
First, nutrient concentrations are very high and
are unlikely to limit primary production, unless
when phytoplankton biomass is very high. Second,
like in many other freshwater tidal estuaries (e.g.
Heinbokel et al., 1988; Pace et al., 1992; Holst
et al., 1998; Park & Marshall, 2000), the zooplankton community in the freshwater tidal
reaches of the Schelde estuary is dominated by
rotifers (Muylaert et al., 2000b) while the zooplankton community in the brackish reaches of
estuaries is usually dominated by marine calanoid
copepods (Soetaert & Van Rijswijk, 1993). As
opposed to marine calanoid copepods, rotifers are
inefficient in controlling phytoplankton biomass
because they are characterised by high threshold
food levels (Walz, 1997) and only graze on small
algae (Rothhaupt, 1990). Finally, even when irradiance and temperature are too low and discharge
is too high to allow for the development of phytoplankton blooms within the freshwater tidal
reaches, phytoplankton biomass can be high due
to import from the tributary Schelde river. This
imported phytoplankton biomass contributes to
primary production in the estuary, especially in the
most upstream stations.
Acknowledgements
The research presented in this paper was carried
out in the framework of the Flemish OMES project (’Onderzoek naar de Milieu-Effecten van het
Sigmaplan’), coordinated by Prof. Patrick Meire.
Stefaan Van Damme is thanked for organising the
sampling campaigns and providing data on salinity and temperature. Peter Herman provided useful comments which improved a previous version
of the manuscript. Koenraad Muylaert is research
assistant for the Fund for Scientific Research
(Flanders). The Fund for Scientific Research is
thanked for funding the Scientific Community
‘Ecological characterization of European estuaries, with emphasis on the Schelde estuary’ (project
nr. W 10/5 – CVW.D 13.816).
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