Freshwater Biology (2003) 48, 404–417
Modelling the impact of benthic filter-feeders
on the composition and biomass of river plankton
J . - P . D E S C Y * , E . E V E R B E C Q †, V . G O S S E L A I N * , L . V I R O U X * AND J . S . S M I T Z †
*URBO, Laboratory of Freshwater Ecology, Department of Biology, University of Namur, Namur, Belgium
†CEME, Institute of Physics, University of Liège, Liège, Belgium
SU M M A R Y
1. The POTAMON model [Everbecq E. et al. (2001) Water Research, 35, 901] has been used to
simulate the effect of benthic bivalves (mainly Dreissena polymorpha) on the phytoplankton
and zooplankton in a lowland Western European river (the Moselle). Here we use a
modified version of the POTAMON model with five categories of phytoplankton
(Stephanodiscus, Cyclotella-like, large diatoms, Skeletonema and non-siliceous algae) to model
filter-feeding effects of benthic bivalves in the Moselle. Zooplankton has been represented
in the model by two categories, Brachionus-like and Keratella-like rotifers.
2. According to density estimates from field surveys (Bachmann V. et al. (1995)
Hydroécologie Appliquée, 7, 185, Bachmann V. & Usseglio-Polatera P. (1999) Hydrobiologia,
410, 39), zebra mussel density varied among river stretches, and increased through the
year to a maximum in summer. Dreissena filtration rates from the literature were used, and
mussels have been assumed to feed on different phytoplankton categories (but less on
large and filamentous diatoms) as well as on rotifers.
3. The simulations suggest a significant impact of benthic filter-feeders on potamoplankton
and water quality in those stretches where the mussels are abundant, their impact being
maximal in summer. Consequently, different plankton groups were not affected to the
same extent, depending on their period of development and on indirect effects, such as
predation by mussels on herbivorous zooplankton.
4. A daily carbon balance for a typical summer shows the effect of benthic filter-feeders on
planktonic and benthic processes: the flux of organic matter to the bottom is greatly
enhanced at high mussel density; conversely, production and breakdown of organic
carbon in the water column are reduced. Mussel removal would drive the carbon balance
of the river toward autotrophy only in the downstream stretches.
Keywords: lowland river, modelling, mussels, phytoplankton, zooplankton
Introduction
Zebra mussels (Dreissena polymorpha Pallas) have
drawn considerable attention to benthic filter feeders
after their recent invasion of large American lakes,
and several studies have reported ecological effects of
benthic bivalves in river systems. The main direct
effect of mussels in freshwater ecosystems is their
Correspondence: J.-P. Descy, URBO, Laboratory of Freshwater
Ecology, Department of Biology, University of Namur, Namur,
Belgium. E-mail: [email protected]
404
predation on plankton. Other effects of dense populations of benthic filters-feeders in rivers are (i) an
increase of oxygen consumption through respiration
of the benthos (Effler et al., 1996, 1998; Bachmann
et al., 1998; Bachmann & Usseglio-Polatera, 1999;
Garnier, Billen & Palfner, 2000), (ii) competition of
exotic species with native unionids for food and
through fouling, leading to their decline, along with
several other changes in the zoobenthos (reviewed for
North American rivers in Strayer & Smith, 1996), and
(iii) resulting from predation on plankton, a channelling of planktonic production to the benthos with
2003 Blackwell Publishing Ltd
Modelling benthic filter-feeders and river plankton
corresponding changes to the food web and carbon
pathways (Welker & Walz, 1998; Jack & Thorp, 2000).
The size range of prey of young and adult zebra
mussels is 20–450 lm, hence they can feed upon most
phytoplankton and small zooplankton (Sprung &
Rose, 1988; Grigorovich & Shevtsova, 1995). Strayer
& Smith (1996) have attributed losses of phytoplankton and zooplankton in several North American rivers
to feeding by this exotic bivalve. Predation on small
zooplankton (including rotifers and nauplii), with
grazing rates similar to those on phytoplankton,
has been demonstrated in the laboratory (MacIsaac,
Lonnee & Leach, 1995) and field (Jack & Thorp, 2000).
Accordingly, data from studies in rivers have shown a
significant impact on phytoplankton and zooplankton. Pace, Findlay & Fischer (1998) reported a >70%
decline in zooplankton biomass (especially of ciliates,
rotifers and nauplii) following invasion by Dreissena
of the Hudson River, along with a 80–90% reduction
in phytoplankton biomass.
Despite their capacity to feed on a wide range of
plankton, zebra mussels filter most efficiently on
particles of 5–35 lm, and filtration rate varies with
body size (Walz, 1978; Young et al., 1996). Several
authors have measured the filtration rate of Dreissena
experimentally and have explored the effects of
mussel size, temperature and food concentration.
For instance, Sprung & Rose (1988) found a typical
functional response with maximum filtration of
230 mL ind)1 h)1 at low food concentration, and a
minimum of 50 mL ind)1 h)1 at high food. Other
published values lie in this range: Reeders, Bij de
Vaate & Slim (1989) measured 78–170 mL ind)1 h)1 by
20–22 mm mussels. According to Walz (1978), the
mean maximum filtration rate is 80 mL ind)1 h)1 and
the incipient limiting level (ILL) is 2 mg C L)1; optimal temperature is 15 C and mussels filter 70% of the
time. Other workers found optimal ingestion and
assimilation rates between 20 and 24 C (Aldridge,
Payne & Miller, 1995). On the other hand, in situ
investigations seem to show an effect of temperature in
relation to seasonality (see Reeders et al., 1989; Fanslow, Nalepa & Lang, 1995; Sprung, 1995). Selectivity
has been rarely reported, although Bastviken, Caraco
& Cole (1998) showed net selective removal of algae,
not related to algal size, in laboratory experiments.
Most studies have dealt with the invading species
D. polymorpha, but a high density of native unionid
mussels can have similar impacts, as described in a
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
405
river-lake system (River Spree, Germany) by Welker
& Walz (1998). In most cases in Europe, however, the
proliferating bivalves are exotic. The most famous is
Corbicula sp., which lives on a wide range of substrata
(Bachmann et al., 1995, 1997), and possibly competes
with Dreissena for space and resources. The filtration rate of Corbicula on phytoplankton is about
50 mL ind)1 h)1 (Boltovskoy, Izaguirre & Correa,
1995), and seems non-selective, despite the fact that
diatoms and Chrysophytes were found in greater
abundance in the mussels’ digestive tracts. In North
America, phytoplankton depletion following invasion
by the exotic bivalve Corbicula fluminea (Müller) was
observed in the Potomac River in the early 1980s
(Cohen et al., 1984).
Some simulation models have been developed to
predict the effects of mussels on freshwater communities and ecosystems. For instance, Padilla et al.,
(1996) used a model for investigating zebra mussels
impact in Green Bay, Lake Michigan. They predicted a
greater impact on large phytoplankton than on small,
as small algae may compensate for grazing losses by
enhanced growth, owing to an increase in phosphorus
cycling and in water clarity. Cladocerans feeding
mainly on small phytoplankton were not greatly
affected by zebra mussels. Overall, these authors held
the view that the ecological effects of invasion in
North American lakes may be less than expected.
Caraco et al. (1997) developed a box-flow model of the
Hudson River and demonstrated that grazing by
dense zebra mussel population is likely to result in
low algal biomass. Indeed, in the light-limited conditions prevailing in turbid, nutrient-rich rivers, zebra
mussel filtration does not improve water clarity to the
extent that phytoplankton could compensate for
grazing losses. Furthermore, the concentration of
suspended solids in rivers (in the 10 mg L)1 range)
does not affect the filtration activity of the molluscs.
For these reasons, it seems that rivers may be more
sensitive than lakes to development of dense mussel
populations and to dramatic plankton decline (Gosselain et al., 1998b). Garnier et al. (2000) applied the
RIVERSTRAHLER model to the River Moselle and its
tributaries, and showed the effect of filter feeders on
total chlorophyll a and on the oxygen budget. They
demonstrated that a low summer oxygen concentration in some river stretches results from high organic
matter loading, reduced phytoplankton biomass and
respiration by the macrozoobenthos.
406
J.-P. Descy et al.
Here we apply a non-stationary river plankton
model, POTAMON, which was developed for predicting potamoplankton composition and biomass
(Everbecq et al., 2001). We use model simulations
and data on the plankton of the River Moselle in 1993
to explore the effects of benthic grazers on plankton
composition and biomass. In particular, we consider
mussels as feeding on different categories of phytoplankton and on herbivorous rotifers. We also
investigate some impacts on ecosystem function.
Methods
Site description and ecological characteristics
A 200-km stretch of the river Moselle was studied
(Fig. 1), from Frouard in France (river km 183) to
Detzem in Germany (river km 376), from 1993 to 1995.
Various environmental, water quality and plankton
data were collected in each year at several sites over
the growing season (see Gosselain et al., 1998b).
Details of the potamoplankton (phyto- and zooplankton) composition and biomass can be found in
Gosselain (1998) and Viroux (1997), along with methods of sampling and data acquisition. Briefly, 1993
was characterised by differences in the development
of the potamoplankton at different points along the
river. In the upstream reach (i.e. up- and downstream
of the city of Nancy), phytoplankton biomass varied
little over the growing period; zooplankton peaked in
spring, and again more strongly in summer. In the
downstream reach (around Metz and downstream),
the plankton was abundant in spring, with the highest
peaks of both phyto- and zooplankton observed in
early June, but declined sharply in summer and
autumn. Gosselain et al. (1998b) hypothesised that
filtration by zebra mussels and other benthic filterfeeders abundant in this downstream reach could
cause the summer decline of potamoplankton in the
River Moselle.
Composition, abundance and biomass estimates of
the macrozoobenthos for the same period were published in Bachmann et al. (1995, 1997), Bachmann &
Usseglio-Polatera (1999) and Bachmann (2000). In the
period 1993–95, the filter-feeders were dominated by
zebra mussels with some Asiatic clams (Corbicula
spp.), together comprising 75% of macrozoobenthic
biomass. Maximum recorded mussel abundance on
substrata in the main channel was about 7000 m)2 (in
Fig. 1 Location map of the studied stretch of the River Moselle.
the vicinity of Metz and downstream, but was
lower between Nancy and Metz; Fig. 1). Accordingly,
average mussel biomass ranged between 5 and
20 g C m)2, for the whole river bed, depending on
the stretch and the time of the year (see below). The
same range in mussel biomass was used for modelling
purposes by Garnier et al. (2000) in the River Moselle
and by Schöl et al. (2002) in the River Rhine.
Implementation of the model
The POTAMON model has been described in detail in
Everbecq et al. (2001). Except for the inclusion of the
benthic filter-feeders and the different categories of
phytoplankton, the model used here is essentially
the same, using as input data the River Moselle’s
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
Modelling benthic filter-feeders and river plankton
(a)
At 0.5 mg C L–1
4000
3000
Filtration rate (mL g C–1 h–1)
2000
1000
0
5
10
15
20
25
30
Temperature (°C)
At 20 °C
(b)
4000
3000
2000
1000
0
1
2
3
4
5
6
7
–1
Algal biomass (mg C L )
Fig. 2 Dependence of zebra mussel filtration rate
(mL g C)1 h)1) on algal biomass (a) and temperature (b) as
calculated by the model (equations and parameters in Tables 1
and 2, respectively), based on experimental data of Bachmann
(2000) and other references (see text).
characteristics. Morphometric data (slope and width
of the river, presence and characteristics of weirs)
were available at a scale of a few km. We used mean
daily discharge and temperature just upstream the
Cattenom Power plant, and hourly or semihourly
solar radiation measured at Florange (by Meteo
France) and at Trier (by the Deutscher Wetterdienst).
A few changes were made in the POTAMON model
in order to describe adequately the River Moselle
phytoplankton, where the filamentous diatoms Skeletonema potamos (Weber) Hasle and S. subsalsum
(A. Cleve) Bethge develop significant numbers. As
Skeletonema spp. usually achieve maximum biomass in
summer, they were described by physiological and
growth parameters similar to those for green algae,
but with Si required for their growth. The five algal
categories considered in the model predictions are:
(1) Stephanodiscus hantzschii, which is assumed to
represent the following taxa: S. invisitatus Hohn &
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
407
Hellermann, S. hantzschii Grun., S. hantzschii fo. tenuis
(Hust.) Håkansson & Stoermer and S. minutulus
(Kütz.) Round.
(2) Small centric diatoms, or Cyclotella-like, to represent Cyclotella meneghiniana Kütz., Cyclostephanos
dubius (Fricke) Round, and other ‘small’ Thalassiosiraceae.
(3) Large centric diatoms, corresponding to Aulacoseira spp. and large Thalassiosiraceae.
(4) Non-siliceous algae, as a broad category for
describing green algae (mostly Chlorococcales) and
Cryptophytes.
(5) Skeletonema, which includes essentially S. potamos and S. subsalsum.
As for the zooplankton, the model describes two
categories of rotifers, Brachionus-like and Keratellalike rotifers, differing mainly in size, filtration rate
(Gosselain et al., 1996) and general food preferences
(Pourriot, 1977). A similar distinction was successfully
applied in previous analyses of riverine rotifer populations (Gosselain et al., 1996). Indeed, rotifers dominate the zooplankton in the River Moselle, although
small cladocerans may occasionally be abundant
(Viroux, 1997). In eutrophic lowland rivers, rotifers
may reach a density of thousands per litre in late
spring blooms, and exert a significant grazing
pressure on small phytoplankton (Gosselain, 1998;
Gosselain, Viroux & Descy, 1998a; Gosselain et al.,
1998b): filtration rates measured at high rotifer density
regularly reached 20–30% day)1, and small centric
diatoms, that constituted the bulk of the phytoplankton biomass, were particularly affected.
We added a macrozoobenthos compartment, which
was essentially composed of Dreissena-like filter feeders. The biomass of the molluscs was set according to
the available data for the river (see above). Unlike
Schöl et al. (2002), we did not describe explicitly the
population dynamics of the mussels, considering that
the data available on both in situ growth and colonisation were insufficient. Rather, we used an average
minimum value for winter biomass and allowed the
mussel biomass to increase according to a simplified
profile, involving a linear increase up to a summer
maximum of 3.5 times the winter biomass; thereafter,
Dreissena biomass was assumed to decline linearly
back to winter values. This seasonal pattern was
suggested by the detailed study in the River Rhine by
Schöl et al. (2002). Although mussel biomass was not
computed explicitly, oxygen consumption because of
J.-P. Descy et al.
Chl a (µg L–1)
Frouard
180
160
140
120
100
80
60
40
20
0
J
F
M
A
M
J
J
A
S
O
N
D
A
M
J
J
A
S
O
N
D
M
J
J
A
S
O
N
D
M
J
J
A
S
O
N
D
Chl a (µg L–1)
Hauconcourt
180
160
140
120
100
80
60
40
20
0
J
F
M
Koenigsmacher
Chl a (µg L–1)
their presence was split between true respiration,
which depended on temperature and mussel biomass,
and oxygen consumption from the degradation of
mussels faeces, which was related to the amount of
planktonic biomass ingested.
We used a filtration rate of 3600 mL g C)1 h)1, which
is derived from the literature (Walz, 1978), corresponding to 20 C for adult mussels of average size and
biomass feeding 14–15 h day)1. Parameters describing
the dependence of the filtration rate upon temperature
and food concentration were chosen (see Table 2) in
accordance with experimental data (Bachmann, 2000).
We chose an optimal filtration rate at 25 C, although
the range of optima found in the literature is quite large
(15–27 C), suggesting possible acclimation. A rather
high optimal temperature for ingestion and assimilation
(24 C) was reported by Aldridge et al. (1995). ReedAndersen et al. (2000) used an upper thermal threshold
of 27 C for computing Dreissena activity in Lake
Mendota. We also described the filtration rate as
depending on a saturation constant, according to the
results of Bachmann (2000), who measured a mussel
filtration rate 20% lower at high food than at low food
ration. Figure 2 presents the dependence of the filtration
rate of mussels upon temperature and algal biomass, as
used in our model. As the River Moselle is regulated
and rather intensely navigated, we assumed turbulent
mixing over the whole water column. In other words,
we assumed that the plankton was equally distributed
over the whole river depth and that the zebra mussel
filtration did not affect this distribution.
Tables 1 and 2 summarise the main processes taken
into account in the biological sub-model. Those are
essentially the same as in Everbecq et al. (2001), but
with the addition of the Skeletonema algal category and
of the macrozoobenthos compartment.
For comparison with calculated values, we used:
• Phytoplankton biomass from measured chlorophyll a (Chl a), expressed as lg Chl a L)1 or as
lg C L)1, based on a single C : Chl a ratio of 30
(Gosselain et al., 1998b);
• Carbon biomass of phytoplankton categories,
estimated from relative biomass from microscope
counts and measured chlorophyll a (according to
Gosselain et al., 1998b and Gosselain, Hamilton &
Descy, 2000);
• Biomass of rotifers estimated from counts, using
published values of specific dry weight and conversion to carbon biomass (Viroux, 1997, 2000);
180
160
140
120
100
80
60
40
20
0
J
F
M
A
Sierck
Chl a (µg L–1)
408
180
160
140
120
100
80
60
40
20
0
J
F
M
A
Month
Fig. 3 Simulated (lines) and observed (dots) chlorophyll a in
the studied stretch of the River Moselle in 1993, from the
upstream site (Frouard, top) to the downstream site (Sierck,
bottom).
• Oxygen concentration measured during routine
surveys by the French authorities.
Results
In order to evaluate the effect of mussels on potamoplankton and on ecological processes, the model was
run for the conditions of the year 1993, for the whole
sector of the River Moselle between the source and the
French–German border (km 310). Simulations of the
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
Modelling benthic filter-feeders and river plankton
409
Table 1 Internal fluxes of the plankton sub-model
Description
Units
Equation
Phytoplankton
phyj
Tpphy
Kopt (T)
T
Red_P
PPO4
Red_Si
Phytoplankton concentration
Production rate
Light saturated rate of photosynthesis
Temperature
Phosphorus limitation factor
Phosphates concentration
Silica limitation factor
mg C L)1
s)1
mg C mg C)1 s)1
C
–
mgP L)1
–
f(I)
Light limitation factor
–
I (z,t)
I0 (t)
Ik
wmoy
ke
k1, k2, k3
POC
Tmphy
Trphy
Tsphy
Graz
tfzoophy
tfdressphy
Available light
Incident light energy
Light saturation constant
Average light over the preceding 7 days
Extinction coefficient
Extinction coefficient parameters
Particular organic carbon
Mortality rate
Respiration rate
Sedimentation rate
Grazing rate
Edibility coefficient by zooplankton
Edibility coefficient by mussels
lE m)2
lE m)2
lE m)2
lE m)2
m)1
Zooplankton
Zooi
tfzoom
tfzoo
Zooplankton concentration
Maximum filtration rate
Filtration rate
mg C L)1
L mg C)1 day)1
L mg C)1 day)1
phyG
Grazable phytoplankton
mg C L)1
tfzoom20 Æ qgzoo e[(T)20) ⁄ 10]
tfzoom
tfzoom Æ Cphyzoo/phyG if phyG > Cphyzoo
P
tfzoophyjÆphyj
trzoo
tmzoo
Respiration rate
Mortality rate
s)1
s)1
trzoo20 Æ qrzoo e[(T)20) ⁄ 10]
tmzoo20 Æ qmzoo e[(T)20) ⁄ 10]
Mussels
Dress
Tfiltdrm
Tfiltdr
phytotdr
Kphydr
Mussel concentration
Maximum filtration rate
Filtration rate
Grazable phytoplankton
Saturation constant
mg C m)2
L mg C)1 day)1
L mg C)1 day)1
mg C L)1
mg C L)1
Tfiltdrm Æ (Topt) Æ e[–(T–Topt)2 ⁄ dtek2]
Tfiltdrm Æ Kphydr ⁄ (phytotdr + Kphydr)
P
tfdressphyjÆphyj
s)1
s)1
s)1
s)1
Kopt (T) Æ Red_P Æ Red_Si Æ f(I)
Kopt (Topt) Æ e[–(T–Topt)2 ⁄ dtek2]
PPO4 ⁄ (PPO4 + KPO4)
SiO2 ⁄ (SiO2 + KSiO2)
h
i
R
Iðz;tÞ=ð2IkÞ
I0 ðtÞ
I0 ðtÞekeH
2 H
2
2Ik
H 0 ½1þðIðz;tÞ=ð2IkÞÞ2 dz ¼ keH arctg 2Ik arctg
I0(t) Æ e–ke
Æ z
b0 Æ wmoy ⁄ (b1 + wmoy)
k1+
P
k2j{{phy}}j+k3{{POC}}
j
mg C L)1
s)1
s)1
s)1
s)1
plankton were examined for four sites: Frouard and
Hauconcourt, located at both ends of a stretch where
the bivalve density was low, and Koenigsmacher and
Sierck, in stretches with high mussel density. Simulations without zebra mussels were run, in order to
reveal the changes because of filter-feeders.
Simulations of variations through time at four sites
and comparison with observations
The model provided a satisfactory overall description
of temporal and longitudinal variations in chlorophyll
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
tmphy20 Æ qmphy e[(T)20) ⁄ 10]
trphy20 Æ qrphy e[(T)20) ⁄ 10]
vsphy ⁄ H
tfzoo Æ tfzoophy Æ zoo
j
j
a (Fig. 3). However, it failed to simulate a phytoplankton peak at the beginning of June in a part of the
study stretch. Small centric diatoms were particularly
abundant during this bloom. The fact that this peak
was not observed at the upstream site (Frouard)
indicates that it could have resulted from an advective
input of phytoplankton from the River Meurthe, a
tributary of the River Moselle (Fig. 1). Temporal
variation of the five phytoplankton categories is
shown in Fig. 4 for an ‘upstream’ site (Frouard) and
for the most downstream site studied (Sierck). Here,
the typical sequence of phytoplankton in lowland
Light saturated rate of photosynthesis
Optimal temperature for photosynthesis
Determines the shape of the Kopt: T curve
Parameter of the Ik equation
Parameter of the Ik equation
Specific extinction coefficient
Half saturation constant for P-limited growth
Half saturation constant for Si-limited growth
Silica: carbon ratio in diatoms
Mortality rate (at 20 C)
Respiration rate (at 20 C)
Sedimentation velocity
Edibility coefficient by Brachionus-like
Edibility coefficient by Keratella-like
Edibility coefficient by mussels
Maximum filtration rate for Brachionus-like (at 20 C)
Maximum filtration rate for Keratella-like (at 20 C)
ILL for Brachionus-like
ILL for Keratella-like
Growth yield for Brachionus-like
Growth yield for Keratella-like
Mortality rate (at 20 C) of Brachionus-like
Mortality rate of Keratella-like (at 20 C)
Respiration rate of Brachionus-like (at 20 C)
Respiration rate of Keratella-like (at 20 C)
Edibility coefficient of Brachionus-like by mussels
Edibility coefficient of Keratella-like by mussels
Maximum filtration rate (at topt C)
Optimal temperature for filtration
Determines the shape of the Tfilt: T curve
Saturation constant for mussels filtration
Growth yield of mussels
Respiration rate of mussels (at 20 C)
Phytoplankton
Kopt (at Topt)
Topt
dtek
b0
b1
k2
KPO4
KSiO2
SiO2: C
tmphy20
trphy20
vsphy
tfzoo1phy
tfzoo2phy
tfdressphy
Zooplankton
tfzoo1m20
tfzoo2m20
cphyzoo1
cphyzoo2
yzoo1
yzoo2
tmzoo120
tmzoo220
trzoo120
trzoo220
tfdresszoo1
tfdresszoo2
Mussels
tfiltdrm20
Toptfilt
dtfilt
Kphydr
ydress
trdress20
L mg C)1 day)1
C
C
mg C L)1
0.25
day)1
day)1
day)1
day)1
day)1
0.25
0.40
L mg C)1 day)1
L mg C)1 day)1
mg C L)1
mg C L)1
mg C mg C)1 day)1
C
C
lE m)2 s)1
lE m)2 s)1
m2 mg C)1
mg P L)1
mg SiO2 L)1
mg SiO2 mg C)1
day)1
day)1
m day)1
1.00
1.00
1.00
Units
0.03
0.086
25
15
20
1.70
1.45
2.0
1.5
0.25
0.22
0.13
0.11
0.13
0.11
6.00
14
8
200
20
0.50
0.01
0.02
0.50
0.15
0.15
0.70
0.90
0.90
1.00
Stephanodiscus
hantzschii
Table 2 Parameters of the plankton sub-model. All rates were temperature adjusted assuming a Q10 of 2.0
0.20
0.17
6.00
21
12
250
25
0.50
0.01
0.06
0.50
0.14
0.14
0.80
0.45
0.60
1.00
Small centric
diatoms
0.15
0.13
6.75
24.5
14
350
30
0.50
0.01
0.00
0.00
0.16
0.16
0.50
0.10
0.10
0.50
Non-siliceous algae
0.12
0.10
3.75
28
10
90
10
0.50
0.01
0.10
0.75
0.06
0.06
0.90
0.25
0.35
1.00
Large centric
diatoms
0.15
0.12
6.25
25
10
275
10
0.50
0.01
0.04
0.25
0.16
0.16
0.70
Skeletonema
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J.-P. Descy et al.
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
Modelling benthic filter-feeders and river plankton
Frouard
411
Sierck
–1
Biomass (mg C L )
Stephanodiscus
3
2
1
0
Biomass (mg C L )
1.0
1.5
–1
Biomass (mg C L )
Biomass (mg C L )
1.0
Biomass (mg C L )
Small centrics
2
1
0
–1
Large diatoms
0.5
0.0
–1
Skeletonema
0.0
Non-siliceous algae
–1
Fig. 4 Simulated (lines) and observed
(dots) carbon biomass of the five algal
categories represented in the POTAMON model, at the most upstream
sampling site (Frouard, left) to the most
downstream studied site (Sierck, right)
of the River Moselle in 1993.
0.5
1.0
0.5
0.0
J
F
M
A
M
eutrophic rivers was observed in both simulations and
observations. In particular, there was a large spring
bloom, dominated by Stephanodiscus gr. hantzschii,
followed by an increase of various other centric
diatoms, green algae and cryptophytes (here included
in the non-siliceous algae category). The lack of an
autumn bloom was marked in the River Moselle in
1993, and all groups declined from September
onwards. In the upstream stretch (Frouard, Hauconcourt, see Fig. 3), phytoplankton biomass remained
relatively high throughout the growing season. In
contrast, a summer phytoplankton decline occurred at
the downstream sites, affecting mainly the small
centric diatoms, Skeletonema spp. and the non-siliceous algae.
Zooplankton showed a similar pattern (Fig. 6), with
conspicuous spring maxima and lower biomass
throughout summer. For these organisms, a sharp
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
J
J
A
S
O
N
D
J
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peak in abundance was also observed at the beginning
of June, which was not replicated by the model,
probably because it originated from a upstream
tributary, the River Meurthe (see Fig. 1).
The effect of benthic filter-feeders on
the potamoplankton: simulations without mussels
Comparison of simulations with and without mussels
allows isolation of the effect from all the other factors
that control potamoplankton (Figs 5 and 6). For all
categories, the major impact was seen from June to
September, which may be related to (i) an increase in
filter-feeder biomass; (ii) an increase of their feeding
rate as temperature rises; (iii) lower discharge which
leads to increased predation impact on plankton. For
rotifers, observed and simulated data (Fig. 6) show
the expected downstream increase of biomass, with
J.-P. Descy et al.
412
Frouard
Sierck
Biomass (mg C L–1)
Stephanodiscus
3
2
1
0
Biomass (mg C L–1)
Small centrics
2
1
0
Biomass (mg C L–1)
Biomass (mg C L–1)
Large diatoms
1.0
1.0
0.5
0.0
Skeletonema
0.5
0.0
Biomass (mg C L–1)
Non-siliceous algae
1.5
1.0
0.5
0.0
J
F
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M
J
J
A
S
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N
D
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A
M
J
J
A
S
O
N
D
Fig. 5 Model simulations of the carbon
biomass of the five algal categories represented in the POTAMON model, at the
most upstream sampling site (Frouard,
left) to the most downstream studied site
(Sierck, right) of the River Moselle in 1993.
Black lines: actual situation, with mussels;
grey lines: predicted situation, without
mussels.
Frouard
Sierck
0.8
0.6
0.4
0.2
0.0
Keratella - like
Biomass (mg C L 1)
Fig. 6 Simulated (lines) and observed
(dots) carbon biomass of the two metazooplankton categories represented in the
POTAMON model, at the most upstream
sampling site (Frouard, left) to the most
downstream studied site (Sierck, right) of
the River Moselle in 1993. Black lines:
actual situation, with mussels; grey lines:
predicted situation, without mussels.
Biomass (mg C L 1)
Brachionus - like
0.2
0.1
0.0
J
F
M
A
M
longer retention time allowing more generations to be
produced. The difference between simulations shows
the very strong effect of predation on metazooplankton by mussels in the study stretch. It appears that
J
J
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both rotifer categories were strongly reduced from
June onwards, despite their high potential population
growth. Note that larger zooplankton, although present, were usually scarce, with the small cladoceran
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
Modelling benthic filter-feeders and river plankton
Bosmina longirostris (Müller) reaching biomass maxima
at about 0.05 mg C L)1. Among phytoplankton
(Fig. 5), two contrasting patterns can be identified.
Two algal groups, Stephanodiscus and the ‘small centrics’, were only slightly affected by mussel predation,
although all algae were described as 100% edible by
the bivalves. The remaining algal groups were much
more affected by mussel feeding activity (Fig. 5). The
model simulations indicated that these algae would
have maintained higher biomass without the high
density of benthic filter-feeders.
Simulations of heterotrophic activity, oxygen
and extinction coefficient
Built as an ecological model which describes all
important processes in the river ecosystem, POTAMON enables us to explore the impact of benthic
filter-feeders on ecosystem function and water quality. Figure 7 presents the simulations of chlorophyll a,
heterotrophic bacteria, light attenuation in the water
column and dissolved oxygen at both ends of the
studied stretch of the River Moselle. The removal of
plankton biomass from the water column by benthic
Fig. 7 Model simulations of chlorophyll a,
heterotrophic bacteria, vertical attenuation coefficient and dissolved oxygen, at
the most upstream sampling site (Frouard,
left) to the most downstream studied
site (Sierck, right) of the River Moselle
in 1993. Black lines: actual situation, with
mussels; grey lines: predicted situation,
without mussels.
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
413
grazers led to two contrasting effects (observed
essentially during the growing season). On the one
hand, the biomass of heterotrophic bacterioplankton
was reduced, as less dissolved organic carbon (DOC)
available to bacteria was released in the water by
phytoplankton excretion and mortality (Descy et al.,
2002). On the other hand, water transparency was
somewhat improved by the decrease of algal biomass,
particularly in the downstream part of the river,
which supported a high density of filter-feeders. With
regard to the oxygen budget, the simulated removal
of benthic grazers increased dissolved oxygen concentration at the downstream site from June to
September. These results clearly show that, although
water transparency was increased by filter-feeder
activity, light penetration remained in the range
limiting to photosynthesis. This was attributable to
the high inorganic turbidity of such large river
systems. The relative improvement in light penetration did not compensate for the decrease in autotrophic biomass from mussel grazing. Also, the
oxygen budget was affected by mussel metabolism
and increased organic matter degradation in the
sediment (see below).
J.-P. Descy et al.
414
Effect of mussels on the organic carbon transfer
between compartments in the river ecosystem
We calculated carbon fluxes, with and without mussels, at the two ends of the study stretch of the River
Moselle (Fig. 8) for a typical summer day. At the
upstream site (Frouard, with low mussel density),
mussel predation resulted in a slight reduction in
production and respiration, as well as in organic
matter breakdown by the heterotrophic bacteria in the
water column. Conversely, more organic matter was
broken down and consumed on the bottom as a result
of mussel activity. These changes in carbon fluxes were
much stronger in the downstream site, where there
were abundant benthic filter-feeders. Note, however,
that photosynthetic production was reduced proportionately less than algal respiration. With regard to the
balance of autotrophy versus heterotrophy, all sites of
the studied stretch were heterotrophic, depending on
their physical characteristics (particularly from the low
Frouard (low mussel density)
5
Without mussels
With mussels
4
Organic carbon flux (g C m 2 day 1)
3
2
1
0
Sierck (high mussel density)
5
Without mussels
With mussels
4
3
2
1
0
Phytoplankton
production
Phytoplankton
respiration
OM breakdown in OM breakdown /
the water column consumption on
the bottom
Fig. 8 Organic carbon fluxes in the two extreme sites of the
studied stretch of the River Moselle, for the Julian day 228, 1993,
as simulated by the POTAMON model. White bars: simulated
situation without mussels; grey bars: simulated situation with
mussels. OM ¼ organic matter.
euphotic depth: total depth ratio, which limits primary
production). Removal of mussels would not greatly
affect this balance in the upstream part of the river,
while downstream the balance would be improved
toward autotrophy. At Sierck, for instance, the carbon
production: carbon consumption ratio would change
from 0.42 to 0.69, and the organic carbon transfer to the
benthic compartment would be reduced about threefold.
Discussion
Regarding changes in ecosystem functions in lowland
rivers brought about by the development of large
populations of zebra mussel and other benthic grazers, we have reached similar conclusions to other
authors. Garnier et al. (2000) identified zebra mussel
predation as the main cause for the decline of chlorophyll a in the R. Moselle where it is heavily colonised by D. polymorpha and other benthic grazers.
They proposed that the balance between autotrophy
and heterotrophy varied in successive river stretches.
Schöl et al. (2002) refined the description of zebra
mussel population dynamics in the River Rhine,
showing that grazing by benthic filter-feeders exhibited strong seasonal variations and greatly exceeded
grazing by metazooplankton in summer. However,
total calculated grazing in the River Rhine reached a
maximum of 0.2 days)1, which is much less than in
other rivers, where both rotifer and benthic grazer
abundance may be higher. For instance, Gosselain
et al. (1998a) measured rotifer grazing rates up to 0.32
(1994) and 1.13 days)1 (1996) in the River Meuse, and
Bachmann et al. (1998) estimated that 57% of the
water volume may be filtered by the macrobenthos of
the River Moselle. Caraco et al. (1997) explored the
sensitivity of the River Hudson ecosystem to the zebra
mussel invasion with a mechanistic model and were
able to demonstrate that the dramatic phytoplankton
decline observed over several years resulted entirely
from zebra mussel grazing. They emphasised that
river depth, complete mixing of the water column,
high nutrient concentration and high inorganic (nonphytoplankton) turbidity are characteristics of lowland rivers that render them sensitive to invasion by
zebra mussels. For instance, nutrients and turbidity
cannot be influenced by the organisms to a point
where there could be some compensation for zebra
mussel predation, as is observed in lakes.
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
Modelling benthic filter-feeders and river plankton
Our application of the POTAMON model to the
River Moselle in 1993 supports these conclusions.
Moreover, we draw attention to the role of flow rate
in a river system, which influences many processes,
including the impact of benthic grazers on phytoplankton. Indeed, keys to understanding the strong seasonal
differences in the impact of mussel grazing may be
population dynamics (Schöl et al., 2002) and temperature dependence of the filtration rate, as well as the fact
that, at lower discharge, residence time increases,
allowing a greater volume of water to be filtered per
unit time. Accordingly, ecological effects are major in
summer as seen for instance on chlorophyll a and
dissolved oxygen. As in the case of the River Hudson,
improved water clarity has little effect on photosynthesis and phytoplankton growth in the River Moselle.
This contrasts with lakes that have been invaded by the
zebra mussel, where some of the grazing losses may be
compensated by enhanced growth rate (Padilla et al.,
1996; Reed-Andersen et al., 2000) from improved water
transparency and nutrient cycling.
In addition, our plankton sub-model has enabled us
to describe with more detail the impact of filterfeeders on the whole potamoplankton community,
and to explore their effects on the planktonic food web
in a lowland river. A high density of mussels, filtering
actively as temperature increased, suppressed the
density of rotifers in summer, as in other rivers, e.g.
the River Meuse (Viroux, 2000). As observed in the
laboratory (MacIsaac et al., 1995) and in enclosure
experiments in the Ohio River (Jack & Thorp, 2000),
rotifers can be ingested by zebra mussels and mussel
invasions may lead to a spectacular decline of small
zooplankton in rivers (Pace, Findlay & Fischer, 1998).
Rotifers usually constitute the bulk of metazooplankton in lowland rivers, where short residence time does
not allow large crustaceans to develop. Predation on
rotifers by benthic filter-feeders is likely to lead to
alterations of food web interactions within the plankton, which may affect the whole river food web. As
shown by field observations and by the results of our
modelling study, rotifers are particularly sensitive to
mussel predation. It is interesting to note that the
zooplankton declined proportionately more than the
phytoplankton, despite the fact that the predation
coefficient of filter-feeders on rotifers in the model
was lower. The reason for this is that zooplankton
grows more slowly, and cannot compensate for predation losses.
2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 404–417
415
Similar community changes brought about by grazing of the zoobenthos can be seen in the phytoplankton, although with strong differences among algal
categories. Whereas all phytoplankton may be equally
grazed by mussels, based upon the settings of the
model, different algae were not affected in the same
way. On one hand, Stephanodiscus escaped predation
because it developed in spring, when mussel biomass
and temperature were still low, so that total activity of
filter-feeders was low and their overall impact on the
water column reduced by high flow rate. Some algae
like ‘small centrics’, on the other hand, although
preyed upon by mussels at the same rate as other
algae, may have benefited from the simultaneous
reduction of herbivorous zooplankton. In other
words, it is likely that compensatory effects occurred
for these diatoms, and that their conspicuous downstream decrease (Fig. 4) was because of factors other
than grazing and predation, i.e. other losses and ⁄ or
competition with other algal groups. The remaining
algal groups were much more affected by mussel
feeding activity (Fig. 5). These algae, i.e. colonial
green algae, large unicellular and filamentous diatoms, are usually less sensitive than small centric
diatoms to rotifer grazing and thrive in lowland rivers
such as the Meuse in summer (Gosselain et al., 1998a).
In contrast, they have declined spectacularly in stretches of the River Moselle heavily colonised by benthic
filter-feeders. To summarise the effect of high zebra
mussel density on the river plankton, spring blooms of
diatoms and rotifers persist, whereas part of the algae
and virtually all small zooplankton are lost in summer.
This is a dramatic situation, which may affect the entire
food web in lowland river systems, in ways which have
not yet been fully evaluated.
Acknowledgments
The field study on the River Moselle (1993–95) was
funded by the CIPMS-IKSMS (International Commission for the Protection of the Moselle and Saar rivers).
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(Manuscript accepted 15 September 2002)