Freshwater Biology (2002) 47, 2380–2387
Short-term and long-term effects of zooplanktivorous fish
removal in a shallow lake: a synthesis of 15 years of data
from Lake Zwemlust
W O U T E R J . V A N D E B U N D * and E L L E N V A N D O N K
NIOO Center for Limnology, Rijksstraatweg, Nieuwersluis, The Netherlands
*Present address: European Commission, Joint Research Centre, Institute for Environment and Sustainability, T.P. 290, 21020
Ispra (Varese), Italy.
SU M M A R Y
1. Removal of zooplanktivorous fish (mainly bream) in 1987 from a shallow eutrophic lake
in the Netherlands, Lake Zwemlust, resulted in a quick switch from a turbid state with
cyanobacteria blooms to a clear state dominated by macrophytes.
2. The clear state was not stable in the long term, however, because of high nutrient
loadings.
3. In 1999, another removal of zooplanktivorous fish (mainly rudd) had similar effects as
in 1987, although macrophytes returned more slowly.
4. In the years directly following both interventions there was a ‘transition period’ of very
clear water with high densities of zooplanktonic grazers in the absence of macrophytes;
low oxygen concentrations indicate that during those years primary production was low
relative to heterotrophic activity.
5. The transition period appears to provide the light climate necessary for the return of
macrophytes.
6. Reduction of nutrient loading is necessary to improve water quality in Lake Zwemlust
in the long term. In the short term, repeated fish stock reduction is a reasonable
management strategy to keep Lake Zwemlust clear.
Keywords: alternative stable states, biomanipulation, food web interactions, lake management,
macrophytes
Introduction
The relation between nutrient availability and phytoplankton biomass in shallow lakes is not straightforward, because the relative importance of top-down
and bottom-up controls can vary widely between both
lakes and years (Jeppesen et al., 1997). Positive feedback mechanisms that tend to stabilise either a clear,
macrophyte-dominated state, or a turbid state characterised by algal blooms have been identified within
a certain range of nutrient conditions (Timms & Moss,
1984; Scheffer et al., 1993). The stability of both
Correspondence: Wouter J. Van de Bund, NIOO Center for
Limnology, Rijksstraatweg 6, 3631AC Nieuwersluis, The
Netherlands. E-mail: [email protected]
2380
situations depends upon many factors, including
lake morphology (Benndorf, 1995), nutrient loading
(Hosper, 1998; Jeppesen et al., 1999), climate (Jayaweera
& Asaeda, 1995), and food web structure (Klinge,
Grimm & Hosper, 1995). The concept of multiple
stable states in shallow lakes (Scheffer et al., 1993) has
proved to be very useful for water quality management. Many lake restoration projects have demonstrated the possibility to induce a switch in shallow
lakes from the turbid to the clear state by food web
manipulation (see reviews by Perrow et al., 1997;
Hansson et al., 1998).
The presence of macrophytes is usually the key
factor stabilising the clear state in the long term (Van
Donk et al., 1993). Macrophytes are considered superior competitors for nutrients compared with algae
2002 Blackwell Science Ltd
Biomanipulation of Lake Zwemlust
(Kufel & Ozimek, 1994). In contrast to phytoplankton,
many macrophytes may access nutrients in the
sediment (Barko & James, 1998), and increased
denitrification in macrophyte beds may impose an
additional constraint on algal growth (Meijer et al.,
1994). Zooplankton grazing on phytoplankton is also
enhanced within macrophyte beds, because macrophytes offer the grazers shelter from planktivorous
fish (Timms & Moss, 1984). Finally, allelopathic
substances released by macrophytes can have a
negative impact on phytoplankton, although the
ecological significance of this mechanism is still
unclear (reviewed by Van Donk & Van de Bund,
2002). Stabilisation of the sediment caused by the
presence of macrophyte beds additionally contributes
to clear water (Barko & James, 1998).
The most difficult part in the restoration of shallow
lakes usually is not to induce a switch to clear water,
but to maintain the clear state in the long term. In many
cases, lakes returned to the turbid state within a few
years after food web manipulation, especially when
nutrient loadings remained high (Jeppesen et al., 1997).
The Dutch Lake Zwemlust is a good example of an
initially successful food web manipulation (Van Donk
& Gulati, 1995; Van Donk, 1998), where the macrophyte-dominated state was unstable in the long term.
In this paper we summarize the developments in
Lake Zwemlust in the period 1986–2000. This period
includes two biomanipulations, in 1987 and 1999. Our
objectives are (i) to identify the main factors responsible for the return of the lake to the turbid state
following the first intervention by analyzing long-term
monitoring data (2) to evaluate the short-term effects
of food web manipulation by comparing the response
of key variables to the two interventions, and (3) to
make recommendations for management strategies for
Lake Zwemlust and comparable small lakes.
Methods
Study area
Lake Zwemlust is a small water body (area 1.5 ha;
mean depth 1.5 m), situated in the middle of the
Netherlands. It receives high external P and N loadings
estimated at about 2 g P m)2 y)1 and 9 g N m)2 y)1, by
seepage from the River Vecht running about 50 m from
the lake. Before the biomanipulation in 1987, phytoplankton blooms were observed throughout the year
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387
2381
(Secchi depth 0.3 m). Detailed descriptions of the
limnology of the lake, before and after the first
biomanipulation in 1987, are given in Van Donk et al.
(1990a, 1993) and Van Donk & Gulati (1995).
Interventions
In March 1987, the lake was drained within four days
by pumping out the water. The whole fish community,
weighing c. 1000–1500 kg and comprising about 75%
bream (Abramis brama L), was removed by seine and
electrofishing. It was anticipated that fish would
eventually recolonise the fishless lake, for example as
egg-material transported by birds. Therefore, it was
decided to create and maintain an abundant 0+ pike
population. After the lake got refilled by seepage
(c. 3 days), it was restocked with 1600 artificially
propagated 0+ pike (Esox lucius L) measuring 4 cm and
with 140 rudds (Scardinius erythrophthalmus L) measuring 9–13 cm fork length. The introduced rudd had
well developed gonads. The offspring was meant to
serve as food for pike. Small plants of Chara globularis
(Thuill.) and 200 rhizomes of Nuphar lutea (L) were
introduced. A total of 170 stacks of willow twigs were
fixed to the bottom to provide refuge and spawning
grounds for pike and as shelter for zooplankton (for
further details see Van Donk et al., 1990a).
Because the water quality in the lake deteriorated
again in the late 1990s (see Results section), it was
decided to undertake another biomanipulation in late
April 1999. The intention was to drain the lake again
completely and to remove all fish. However, because
of logistical problems, it was only possible to lower
the water level by c. 1 m. As much of the fish stock as
possible was removed by seine fishing. The total
removed biomass was about 150 kg, comprising
almost exclusively rudd. None of the additional
measures taken in 1987 were repeated in 1999.
Monitoring data
The developments in Lake Zwemlust have been
monitored from 1986 onwards. The sampling frequency for determining water chemical parameters,
Secchi depth, chlorophyll-a concentration, and
zooplankton and phytoplankton composition varied
between seasons and years, but samples were taken at
least monthly. The methods are described in detail in
Van Donk, Gulati & Grimm (1990b) and Van Donk
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W.J. Van De Bund and E. Van Donk
et al. (1993). Fish biomass and composition were determined at about yearly intervals in autumn using a
modified mark-recapture method by Peterson (Ricker,
1975; Meijer et al., 1995). No fish data are available for
the years 1994, 1996 and 1997. In 1998, fish biomass
was estimated indirectly using data from the 1999
sampling and the removed fish biomass during
biomanipulation. Abundance of herbivorous and
omnivorous waterfowl was recorded at each sampling
occasion. Biomass and composition of submerged
macrophytes in the lake were estimated yearly in late
summer; a detailed description of the methods is
given in Ozimek, Gulati & Van Donk (1990).
Results
Long-term developments
Before the interventions of 1987, the lake was characterised by very low water transparency with chlor-
ophyll-a concentrations up to 250 lg L)1. In summer,
the phytoplankton was dominated by cyanobacteria.
Macrophytes were totally absent. After the interventions, the water became clear almost immediately.
Secchi disc measurements showed almost continuous
bottom sight during the period 1988–91 (Fig. 1a).
Chlorophyll-a concentrations were relatively low
(Fig. 1b). Cyanobacteria were almost absent during
those years, whereas cryptophytes were relatively
abundant (Fig. 2). From 1992 to 1995, alternations of
periods with clear and turbid water occurred within
the same year, and cyanobacterial blooms started to
reoccur. A detailed analysis of changes in phytoplankton composition is presented in Romo et al. (1996). The
situation deteriorated further from 1996 to 1998; at
the end of that period, the situation was similar to the
situation immediately before the biomanipulation in
1987. The second intervention in 1999 resulted again in
a striking increase of water transparency, similar to the
one observed in 1987 (Fig. 1a).
Fig. 1 Secchi depth (a), Chlorophyll-a
(b), inorganic phosphorus (c) and nitrate
(d) concentrations in Lake Zwemlust in
1986–2000. Dashed lines show the dates of
fish removal.
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387
Biomanipulation of Lake Zwemlust
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Fig. 2 Phytoplankton and zooplankton in
Lake Zwemlust in 1986–2000. Phytoplankton panels show the contribution of
cyanobacteria (a), green algae (b), diatoms
(c), cryptophytes (d), and other algae (e) to
total phytoplankton abundance.
Zooplankton panels show the abundance
of large (>500 lm) crustacean zooplankton (f), small (<500 lm) crustacean
zooplankton (g), and rotifers (h). Dashed
lines show the dates of fish removal.
Zooplankton density
(ind. L–1)
Phytoplankton composition
(Percentage of total abundance)
(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
Inorganic nutrient levels showed a rather consistent
seasonal pattern throughout the observation period,
with no obvious effect of the interventions. Soluble
reactive phosphorus (SRP) concentrations were continuously very high (>0.2 mg L)1); there appears to be
a slight tendency to decreasing SRP concentrations
during the period 1993–99 (Fig. 1c). Nitrate concentrations were always high during winter, with a steep
decrease in the spring (Fig. 1d) towards concentrations limiting algal growth (Van Donk et al., 1993).
Zooplankton abundance and composition show a
clear long-term development (Fig. 2). In the years
following the biomanipulation of 1987, the zooplankton was dominated by large species (mainly Daphnia
magna Straus.), with rather high densities during
spring and summer (up to c. 500 ind L)1). In 1990,
small taxa (Ceriodaphnia spp., Bosmina spp.) appeared,
initially at very low densities. From 1990 to 1993, large
and small taxa were both abundant. From 1995 to
1999, large cladocerans were almost absent, and small
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387
cladocerans became extremely abundant during most
of the year, coinciding with high chlorophyll concentrations (Fig. 1b). Very soon after the intervention in
1999, large cladocerans (mainly D. magna) returned,
and the smaller taxa almost disappeared again.
Rotifer densities (Fig. 2h) were rather low in the years
following the biomanipulation in 1987, but became
more abundant in the years 1994–99.
Macrophytes were initially absent, but appeared
very quickly after the intervention in 1987 (Fig. 3). The
plants reached a peak biomass of 170 g dry
weight m)2 in 1989. From 1989 to 1993, their biomass
declined, followed by two additional years characterised by a high biomass. In 1996, the macrophyte
biomass eventually decreased to very low levels and
by 1998 had declined to zero. There was a clear
succession of macrophyte taxa (Fig. 3). Initially the
plant biomass was dominated by Elodea nuttallii
(Planchon). From 1990 to 1991, Ceratophyllum demersum (L) became dominant, followed by 3 years of
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W.J. Van De Bund and E. Van Donk
Fig. 3 Macrophyte biomass and coot density in Lake Zwemlust
in 1986–98. E.n.: Elodea nuttallii; P.b.: Potamogeton berchtoldii;
C.d.: Ceratophyllum demersumi.
Potamogeton berchtoldii (Fieb.) dominance. In 1995,
Elodea returned briefly, reaching a biomass as high as
that in 1989, but then declined quickly.
The macrophytes in Lake Zwemlust attracted high
numbers of grazing birds, mainly coots (Fulica atra
L.; Fig. 3). However, coots did not appear during
the first years after macrophyte recolonisation, but
only in 1989, when the macrophytes had already
reached a high biomass (Fig. 3). Coots were especially abundant in 1989–91 and in 1995–97. These
were all years in which the macrophyte biomass
was dominated by Elodea or Ceratophyllum. In the
Potamogeton-dominated years 1992–94, coots were
almost absent.
In 1986, the fish biomass in Lake Zwemlust was
extremely high and dominated by bream (Van Donk
et al., 1990b). The removal of bream in 1987 was
successful; until the end of the sampling period in
2000, the species was never found again. Rudd,
which was stocked to the lake in 1987, became the
dominant fish species. The rudd population increased
greatly from 1987 to 1990, reaching an estimated
maximum biomass of 550 kg ha)1 (Fig. 4). In subsequent years, the biomass remained rather constant at
this level, at least until 1995. No fish data are
available for the years 1994, 1996 and 1997 and the
results of the 1998 fish sampling are not reliable,
because too few marked fish were recaptured.
However, based on the 1999 fish sampling and the
removed fish biomass during the biomanipulation,
we estimate that rudd biomass before 1999 was at
least 200 kg ha)1, excluding young of the year. These
data suggest that the fish biomass had declined
considerably during the years of phytoplankton
dominance (1996–98).
Fig. 4 Macrophyte and total estimated rudd biomass in Lake
Zwemlust in 1986–98. E.n.: Elodea nuttallii; P.b.: Potamogeton
berchtoldii; C.d.: Ceratophyllum demersum. The rudd biomass in
1998 was estimated from gill-net catches and removed fish
biomass in 1999.
Short-term effects of fish removal
This section provides a more detailed comparison of
the short-term responses to the biomanipulations in
1987 and 1999. Water transparency (Fig. 1b) and
chlorophyll-a concentration (Fig. 1a) showed quite
similar responses in both years. The lake water only
cleared up about 2 months after the lake had filled
again. A spring bloom of green algae occurred 1 year
after the intervention in 1987, whereas no algal bloom
was recorded in the spring following the 1999 intervention (Fig. 1). Cyanobacteria were completely absent
(1987) or only present at extremely low biomass levels
(1999) in the two summers following the interventions.
In 1987, macrophytes returned in the very year of
biomanipulation, increasing to a biomass of as high as
100 g dry weight m)2 in 1988 (Fig. 3). In 1999, the
response was quite different: Even in the summer of
2000, macrophytes were still almost absent, in spite of
extremely clear water. However, a layer of filamentous algae covered the sediment surface of the lake
during most of the summer. By the end of the summer
of 2000, the cover of filamentous algae diminished,
and macrophytes (mainly Potamogeton and Ceratophyllum) started to reappear.
The composition of the zooplankton community
was very similar following the interventions in 1987
and 1999. Densities of large cladocerans were relatively high throughout the season (Fig. 2f), while small
cladocerans (Fig. 2g) and rotifers (Fig. 2h) were virtually absent.
Oxygen depletion occurred following both interventions (Fig. 5). Concentrations decreased to
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387
Biomanipulation of Lake Zwemlust
2385
Fig. 6 Succession of developmental stages in lake Zwemlust
in response to biomanipulation. A: turbid state; B: transition
state; C: clear state; D: clear ⁄ turbid state (see text for
explanation).
Fig. 5 Oxygen concentrations in Lake Zwemlust before and
after the biomanipulations in 1987 (a) and 1999 (b). Dashed lines
show the dates of fish removal.
<3 mg L)1 in the 2 months following the refilling of
the lake. This decline was only observed during the
two postbiomanipulation years, whereas in all other
years oxygen concentrations were near saturation
levels throughout the year. Oxygen depletion was
more severe in 1999 than in 1987. In both years,
oxygen concentrations gradually returned to nearsaturation values in autumn.
Discussion
The long-term data set from Lake Zwemlust presented here does not allow us to separate unambiguously
the two ‘alternative stable states’ that minimal models
predict for shallow lakes (Scheffer, 1990; Scheffer
et al., 1993; Hosper, 1998). Some years can be clearly
characterised as either turbid and phytoplanktondominated (i.e. 1986, 1997, 1998) or as clear and
macrophyte-dominated (i.e. 1989–91). For many other
years, however, it is not possible to place them into
one of these two categories, because they show
characteristics of both.
Figure 6 summarises the developments in Lake
Zwemlust, within the conceptual framework of
‘alternative stable states’. Four different ‘states’ are
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387
distinguished. The turbid (A) and clear (C) states are
separated by two transition periods – the ‘transition
state’ (B) directly following the biomanipulation, and
the ‘clear ⁄ turbid state’ (D) following the clear state.
Biomanipulation appears to induce the ‘transition
state’ (B), where the water is very clear but macrophytes are absent or very rare. This ‘transition state’ is
further characterised by high densities of large daphnids throughout the season, in spite of an extremely
low phytoplankton biomass. The most likely food
source for the daphnids during this time is detritus
and attached bacteria, as has been shown in other
studies (Kamjunke et al., 1999; Picard & Lair, 2000).
The low oxygen concentrations that were measured in
the summers following both biomanipulations (Fig. 5)
indicate that during this phase primary production
was low relative to heterotrophic activity. The ‘transition state’ provides suitable light and nutrient conditions for macrophytes to establish. However,
observations in Lake Zwemlust in the last year of
this study indicate that these conditions may initially
favour filamentous algae and the establishment of
macrophytes may be delayed.
Once macrophytes have reached a high biomass,
the lake enters the clear state (C in Fig. 6). This state
can last for several years. It is characterised by a
relatively high macrophyte abundance during the
whole summer, low algal densities, and high water
2386
W.J. Van De Bund and E. Van Donk
transparency. The situation in this period is not stable
in the long term, however; probably under the
influence of grazing by birds and fish, species shifts
in the macrophyte community were observed, from
Elodea nuttallii to Ceratophyllum demersum to Potamogeton berchtoldii (Van Donk & Otte, 1996; Van Donk,
1998). With the appearance of the latter species, a
‘clear ⁄ turbid’ phase (D in Fig. 6) starts, where periods
of clear water and algal blooms occur within the same
year. One of the factors likely to favour these blooms
is the strong decline of P. berchtoldii in late summer
when the plant starts to form overwintering structures
(Van Donk, 1998). Furthermore, P. berchtoldii is much
more susceptible to periphyton cover than the other
macrophyte species occurring in Lake Zwemlust;
progressive cover with periphyton is considered an
important cause of the decline of P. berchtoldii (Van
Donk & Gulati, 1995). With increasing frequency and
intensity of algal blooms, the lake gradually shifts to
the ‘turbid’ state (A), the only state that appears to be
genuinely stable in Lake Zwemlust.
Ultimately the decline in water quality from the
macrophyte-dominated state to the turbid state is
driven by continuously high nutrient inputs (Timms
& Moss, 1984; Scheffer et al., 1993). The long-term data
presented in this paper do not allow us to identify a
single factor that causes the return to the turbid
situation, but rather several contributing factors can
be recognised. The single most important factor
appears to be the succession in the macrophyte
community towards a dominance of Potamogeton
berchtoldii. Grazing on macrophytes by birds and fish
apparently contributed to this succession of macrophyte species in the lake (Van Donk & Otte, 1996; Van
Donk, 1998). In addition to changes in the macrophyte
community, a shift in the size structure of zooplankton towards smaller taxa (Fig. 2), with a corresponding decrease in grazing potential, appears to be
another important factor fostering the return of
phytoplankton blooms. The cause of the decline of
large daphnids does not become clear from the
available data. However, feeding of planktivorous
fish is not the main reason, because large daphnids
were present until 1994, although rudd had reached a
high biomass already in 1990 (Fig. 4). The refuge
offered by the macrophytes probably protected the
daphnids from effective fish predation (Timms &
Moss, 1984).
The success of fish stock reduction to restore clearwater conditions in Lake Zwemlust with its continuously high nutrient inputs demonstrates the potential
of this measure as a short-term management strategy.
Our data also indicate, however, that the clear state in
this lake with a dominance of macrophytes is not
stable in the long term. As long as nutrient levels are
high, there is a risk that macrophytes will not
successfully establish in a certain year, and if
macrophytes miss their ‘window of opportunity’ to
proliferate on the lake bottom, phytoplankton may
take over again, resulting in a return to the turbid
state. Consequently, reduction of nutrient loading to a
level where the clear, macrophyte-dominated situation is stable is necessary to keep Lake Zwemlust
clear in the long term. As long as the ultimate goal of
reducing nutrient loads is not achieved, repeated fish
stock reduction is a reasonable short-term management strategy.
Acknowledgments
This study was financially supported by the EUEnvironment project SWALE. We would like to
thank S. van Rouveroy van Nieuwaal for compiling
the data set, and Klaas Sieuwertsen for assistance in
the field.
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(Manuscript accepted 31 July 2002)