Freshwater Biology (2002) 47, 24532465

Biomanipulation of lake ecosystems: successful

applications and expanding complexity in the
underlying science
R G E N B E N N D O R F , P E T E R K A S P R Z A K * and R A I N E R K O S C H E L *
THOMAS MEHNER,* JU
*Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany
Dresden University of Technology, Institute of Hydrobiology, Dresden, Germany

SUMMARY
1. To illustrate advances made in biomanipulation research during the last decade, seven
main topics that emerged after the first biomanipulation conference in 1989 are discussed
in relation to the papers included in this special issue and the general literature.
2. The substantially higher success rates of biomanipulations in shallow as opposed to
stratified lakes can be attributed to several positive feedback mechanisms relating mainly
to the recovery of submerged macrophytes.
3. The role of both nutrient loading and in-lake concentrations in predicting the success of
biomanipulations is emphasised and supported by empirically defined threshold values.
Nutrient recycling by aquatic organisms (such as fish) can contribute to the bottom-up
effects on lake food webs, although the degree can vary greatly among lakes.
4. Ontogenetic niche shifts and size-structured interactions particularly of fish populations
add to the complexity of lake food webs and make scientifically sound predictions of
biomanipulation success more difficult than was previously envisaged.
5. Consideration of appropriate temporal and spatial scales in biomanipulation research is
crucial to understanding food web effects induced by changes in fish communities. This
topic needs to be further developed.
6. An appropriate balance between piscivorous, planktivorous and benthivorous fishes is
required for long-lasting success of biomanipulations. Recommended proportions and
absolute densities of piscivorous fish are currently based on data from only a few
biomanipulation experiments and need to be corroborated by additional and quantitative
assessments of energy flow through lake food webs.
7. Biomanipulation effects in stratified lakes can be sustained in the long term only by
continued interventions. Alternate stable states of food web composition probably exist
only in shallow lakes, but even here repeated interventions may be needed as long as
nutrient inputs remain high.
8. Biomanipulation is increasingly used as a lake restoration technique by considering the
needs of all lake users (sustainability approach). The combination of water quality
management and fisheries management for piscivores with positive effects for both
appears to be particularly promising.
9. Biomanipulation research has contributed substantially to progress in understanding
complex lake food webs, which should in turn promote a higher success rate of future
whole-lake biomanipulations.

Correspondence: Thomas Mehner, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Department of Biology and Ecology
of Fishes, POB 850 119, D-12561 Berlin, Germany. E-mail: mehner@igb-berlin.de

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T. Mehner et al.
Keywords: heterogeneity, lakes, maintenance, management, niche shifts, nutrients

Introduction
More than 10 detailed reviews on biomanipulation
have been published since 1990 (e.g. Benndorf, 1990;
Hansson et al., 1998) when the proceedings of the first
international meeting on the topic appeared (Gulati
et al., 1990). This remarkable activity demonstrates the
continuing immense interest in this issue from both a
scientific and practical viewpoint. The focus of the
early reviews was on enclosure and laboratory
experiments. More recently, interest has shifted to
elucidating responses observed after whole-lake
manipulations (Hansson et al., 1998; McQueen, 1998;
Drenner & Hambright, 1999). None of the reviews
leaves a doubt that biomanipulation can be an
effective and powerful tool for water quality improvement. The average success rate of food-web manipulations is about 60% (10 of 17 case studies; Hansson
et al., 1998; 25 of 41 case studies; Drenner &
Hambright, 1999) and only 15% of the whole-lake
biomanipulation experiments (6 of 41 studies)
reanalyzed by Drenner & Hambright (1999) were
considered a definite failure.
Hansson et al. (1998) noted that most of the successful applications were founded essentially on
simple food chain theory (Hairston, Smith & Slobodkin, 1960) and its derivatives such as the biomanipulation concept (Shapiro, Lamarra & Lynch, 1975),
the trophic cascade model (Carpenter, Kitchell &
Hodgson, 1985), the top-down : bottom-up theory
(McQueen, Post & Mills, 1986), and the holistic foodweb model (Persson et al., 1988). Biomanipulation
refers here to the deliberate reduction of planktivory,
which is followed by an increase in the abundance
and size of zooplankton (predominantly large Daphnia
species) and results in increased grazing pressure on
phytoplankton and ultimately clearer water of lakes.
The desired reduction of planktivory may be achieved
either by removing zooplanktivorous fish manually or
by promoting an abundant piscivorous fish community by stocking and protection measures to increase
predation pressure on the planktivorous fish. The
expectation that this simplistic approach works in all
situations is in contrast with the abundance of
publications highlighting the complexity of aquatic
food webs. This suggests that predictions of bioma-

nipulation success may require more detailed understanding of interactions within aquatic food webs.
The results of the first international conference on
biomanipulation held in Amsterdam in 1989 (Gulati
et al., 1990) serve as a starting point to illustrate the
main topics in biomanipulation research about
1215 years ago (Table 1). Many studies focused on
separate trophic levels, such as phytoplankton and
zooplankton, and their links with the trophic levels
adjacent to them. Some detailed attention was given to
species and functional groups that are indirectly
affected by biomanipulation. In addition, the ability
of shallow lakes to switch between two alternate
stable states was clearly expressed, and the limitations
of simple food-chain models to explain some of the
responses observed in lakes were highlighted. Finally,
the potential of biomanipulation for improving lake
water quality was assessed based on the available
empirical and theoretical evidence (Table 1).
Seven partially different themes were identified at
the second symposium on biomanipulation held in
2000 in Rheinsberg near Berlin, Germany (Table 1).
This shift in emphasis is best characterised as an effort
towards a broader, more synthetic view of biomanipulation at the whole-lake scale. This shift was accompanied by and resulted from a large number of
whole-lake biomanipulation experiments, which
replaced the formerly dominating small-scale two-level
experiments.
In this review and synthesis paper, we elucidate the
recent developments in the new topics in some detail
by combining results from papers presented at the
symposium in Rheinsberg and included in this special
issue, and findings from a range of other studies that
have been published mostly since 1990. We will point
out the progress made during the last decade by
relating our conclusions on the current state of
biomanipulation research to the synthesis of the
1989 conference (Lammens et al., 1990).

The distinction between shallow and stratified lakes

There is widespread consensus that biomanipulation
probably has a much higher success rate in shallow
than in stratified deep lakes (Gulati et al., 1990;
McQueen, 1998; Scheffer, 1998). The main advantage

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Biomanipulation today summary and review

2455

Table 1 Summary of the main topics presented at the first biomanipulation conference in 1989 in Amsterdam (synthesis by Lammens
et al., 1990) and the second symposium in Rheinsberg, Germany, as summarised in this special issue
Amsterdam 1989

Rheinsberg 2000

Edibility of phytoplankton
Quality and quantity of phytoplankton
Effects of nutrient concentration on
phytoplankton community structure

Ecosystem stability
Deepwater areas and
macrophytes as refugia
Alternate stable states of shallow lakes

Distinction between shallow and

stratified lakes
Role of macrophytes
Alternate stable states of shallow lakes

Indirect effects
Invertebrate predators
Rotifers
Benthivorous fish phytoplankton link

Biomanipulation and ecosystem

research
Resource-quality response not
predicted by food-chain models
Sizestructured interactions
Stronger role of benthivorous fish

Nutrient supply and recycling

Biomanipulation efficiency
threshold of P-loading
Threshold of in-lake P-concentration
Trophic state of the lake
Nutrient recycling by fish and
zooplankton
Benthivorous fish

The effects of nutrient supply

and recycling on the success
of biomanipulation

Ontogenetic niche shifts and

sizestructured trophic interactions
Ontogenetic niche shifts in piscivores
Role of young-of-the-year fish
Size refuges of prey against
gape-limited predators

The importance of ontogenetic

niche shifts and size-structured
interactions

Temporal and spatial heterogeneity

in food webs
Diel migrations of fish
Littoralpelagic coupling
Benthicpelagic coupling
Timing of predatorprey interactions

The role of temporal variability

and spatial heterogeneity
in food webs

Zooplankton as a key factor

Top-down effects of zooplankton
related to trophic state
Overestimated role of
planktivorous fish
Greater attention directed to
pelagic than benthic zone

Proportion of piscivores to
planktivores benthivores
Role of predatory invertebrates
Balance between piscivores and
planktivores and benthivores
Importance of omnivory
Situation in tropical water bodies

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Topic

The distinction between

shallow and stratified lakes

The relative proportion of

piscivores and planktivores
benthivores in the fish community

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T. Mehner et al.

Table 1 (Continued )
Amsterdam 1989

Rheinsberg 2000

Topic

Management
Assessment of the application
potential of biomanipulation
Role of nutrient supply and
concentration

Long-term maintenance of
biomanipulation
Repeated stocking measures necessary
Drastic manual fish removal required
Press perturbations necessary
Alternative stable states of
food-web configuration

The requirement of long-term

maintenance of
biomanipulation measures

Management and sustainability

Co-operation of all lake users
Water quality and sustainable
fisheries management

The management and

sustainability aspects of
biomanipulation

of food-web manipulations in shallow lakes is the

potential for (re)colonisation of large bottom areas by
macrophytes, which promote the clear-water state of
shallow lakes through a number of mechanisms: (1)
Macrophyte beds can act as a refuge for zooplankton
from fish predation (Stansfield et al., 1997); (2) the
feeding efficiency of predatory fish such as perch
(Perca fluviatilis L.) and pike (Esox lucius L.) in
macrophyte beds is higher than that of planktivorous
or benthivorous cyprinids such as roach [Rutilus
rutilus (L.)] or bream [Abramis brama (L.)] (Winfield,
1986; Grimm & Backx, 1990); (3) experimental and
observational results showing that high densities of
phytoplankton, especially cyanobacteria, rarely occur
when dense macrophyte beds are present suggest that
macrophytes compete with phytoplankton successfully for nutrients (Van Donk et al., 1990) and may
excrete allelopathic substances against cyanobacteria
(Declerck et al., 2000); (4) Conditions inside macrophyte beds may increase denitrification, thus contributing to a decreased availability of nitrogen for
phytoplankton growth (Van Donk et al., 1993); and (5)
resuspension of bottom material is generally lower in
macrophyte beds (Barko & Smart, 1981). All these
mechanisms work together towards stabilising or
even enhancing water clarity, which in turn expands
the water depth and bottom area where macrophytes
can grow. Recognition of this positive feedback
mechanism has led to the theory of alternate stable
states in shallow lakes, with rapid shifts occurring
between a turbid, plankton-dominated state and a
clear, macrophyte-dominated state (Scheffer, 1998).
Shallow lakes in the Netherlands are sensitive to
changes in bream biomass (Lammens, van Nes &
Mooij, 2002). Similarly, long-term data from Lake

Zwemlust (the Netherlands; Van de Bund & Van

Donk, 2002) indicate the switching of shallow lakes
between the turbid and clear-water states, with drastic
fish removals and heavy external nutrient loading
working antagonistically. There is also a convincing
example that stocking of piscivores without manual
removal of planktivores may shift shallow lakes into
the clear state. In Lake Udbyover (Denmark), perch
and pike stocked over a 5-year period induced a
decrease in planktivorous and benthivorous fish
density, which eventually led to the re-appearance
of submerged macrophytes (Skov et al., 2002).

The effects of nutrient supply and recycling

on the success of biomanipulation
It has long been proposed that bottom-up effects of
nutrients on the structure of pelagic food webs remain
effective even in strongly top-down manipulated
lakes (e.g. McQueen et al., 1986). Benndorf (1987)
suggested therefore that the reduction of nutrient
runoff from the catchment may be an important
prerequisite for successful biomanipulation, and that
an annual loading threshold below 0.60.8 g of total
P m)2 of lake surface area must be reached before lake
water quality can be improved by biomanipulation
(Benndorf et al., 2002). Similarly, Jeppesen et al. (1991)
determined an in-lake P-concentration of about
100 lg L)1 as the critical level below which long-term
effects of biomanipulation can be expected in shallow
lakes. Long-term data from Feldberger Haussee,
Germany, a stratified eutrophic hardwater lake, suggest that the improved water quality observed in that
lake over the past 10 years can only partly be
attributed to biomanipulation, because the improve
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Biomanipulation today summary and review

ment concurred with a decline in the nutrient loading
(Mehner et al., 2001). Increasing calcite precipitation
and phosphorus coprecipitation may have further
contributed to the decline in nutrient concentrations
and, indirectly, to the reduction of phytoplankton
biomass in that lake (Koschel, 1997).
In contrast to the findings above, recent studies in
North America, including experiments involving
nutrient additions to lakes, appear not to support the
idea that the P input rate must fall below a certain
threshold for herbivory to control phytoplankton biomass (Carpenter et al., 2001). However, as nutrients
were supplied experimentally only during short dosage periods, the phosphorus accumulation rate of the
sediment was probably higher than under equilibrium
conditions. Therefore, the experiments may not have
mimicked external loading well. In addition, high light
attenuation resulting from high concentrations of coloured DOC (up to 9.5 units m)1) inhibited the development of inedible phytoplankton in those experiments.
The trophic state of lakes has an impact on foodchain length, thus delineating the potential for biomanipulation by changes in the upper trophic levels.
Persson et al. (1992) argued that both oligotrophic and
eutrophic lakes in Europe possess three-level food
chains without piscivores (phytoplankton, zooplankton, planktivorous fish), whereas mesotrophic lakes
have four levels with abundant populations of predatory fish, mainly perch, with a strong top-down
influence on planktivorous roach populations.
According to Persson et al. (1992), the absence of
piscivorous perch in eutrophic lakes is because of the
fact that perch is competitively inferior to roach under
the unfavourable food conditions for perch in eutrophic lakes. A similar argument for stronger top-down
control in mesotrophic lakes was derived from
experimental work on zooplanktonphytoplankton
interactions: Carney (1990) and Elser & Goldman
(1991) proposed the mesotrophic maximum hypothesis stating that the top-down impact on phytoplankton is highest under mesotrophic conditions. In
contrast, Sarnelle (1992) found that Daphnia grazing
on phytoplankton increased with phosphorus
concentration, indicating that the lakes most heavily
impacted by nutrient inputs would show the greatest
response to a reduction in planktivory. Thus, the
hypotheses above predict that the effectiveness of
biomanipulation measures may differ systematically
with the trophic state of lakes.

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2457

A re-discovered effect of biomanipulation is the

enhancement of nutrient recycling by aquatic animals,
including fish, which leads to an indirect bottom-up
influence on pelagic food-web structure. Many effects
of fish on phytoplankton that were originally attributed to the feeding of fish on zooplankton can be
better explained as indirect effects of nutrient excretion and, in part, egestion by fish (Brabrand, Faafeng
& Nilssen, 1990; Schindler et al., 1993; but see
Attayde & Hansson, 2001). Reduced rates of nutrient
recycling resulting from a reduced biomass of
planktivorous fish were apparently responsible for
the success of biomanipulation in the Finnish Lake
Vesijarvi. Zooplankton biomass did not increase in
this lake following biomanipulation (Horppila et al.,
1998), suggesting that biomanipulation success was
mainly triggered by bottom-up forces induced by
intensive fish removal. Similarly, the reduced Precycling after a massive fish kill of the omnivorous
Tilapia and Oreochromis in a shallow tropical reservoir
contributed to a short-term improvement in water
quality (Starling et al., 2002). In contrast, Tarvainen,
Sarvala & Helminen (2002) calculated that P-release
by a roach population could not directly account for
the late summer increase in P concentration observed
in the biomanipulated Lake Koylionjarvi in Finland,
although young fish, which exhibit high metabolic
rates, dominated the population. However, when
growth rates and P demand of roach and the often
very large internal P loading from the sediment
(Sndergaard, Jensen & Jeppesen, 2001) are balanced,
P-recycling by fish may have a low impact on total P
availability in most eutrophic lakes.
Benthivorous fish species such as bream and
common carp (Cyprinus carpio L.) stir up the lake
bottom and thus increase sediment re-suspension,
water turbidity and internal nutrient loading
(Breukelaar et al., 1994). In addition, the feeding
activity of these fishes may directly destroy or uproot
macrophytes, implying that benthivorous fish may
exert bottom-up effects on water quality (Tatrai &
Istvanovics, 1986), and it has been suggested that the
removal of benthivorous fish determines the outcome
of biomanipulation in shallow lakes more strongly
than the removal of planktivorous fish (Lammens
et al., 1990; Drenner & Hambright, 1999). The removal
of cyprinids from Lake Ringsjon, Sweden, resulted in
a rapid change in the diversity of benthic invertebrates, indicating that these fish did indeed disturb

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T. Mehner et al.

the lake bottom, with possible implications for pelagic

nutrient concentrations and the food web (Svensson,
Bergman & Andersson, 1999).

The importance of ontogenetic niche shifts

and size-structured interactions
Body size of organisms is important for determining
the shape and strength of trophic interactions,
particularly in aquatic habitats where size-structured
fish populations dominate (Werner & Gilliam, 1984).
Because single species may show shifts in diet or
habitat use during ontogeny, different developmental
stages must be treated separately when such interactions are analysed. Evidence of ontogenetic niches
comes from fish communities in both North America
(Werner, 1992) and Europe (Persson, 1994). Of
particular interest for biomanipulation is the diet shift
of fish that start their life as planktivores but shift to
piscivory when reaching a certain length (e.g. perch
and pikeperch, Sander lucioperca (L.); Persson,
Bystrom & Wahlstrom, 2000; Beeck et al., 2002).
Establishing a top trophic level of piscivores with
these species therefore entails enhanced planktivory
by the young (Mehner et al., 1996). In addition, as the
abundance of adult planktivorous fishes decreases,
competition for food diminishes, which favours the
recruitment of young stages (Romare & Bergman,
1999). As a result, young-of-the-year (YOY) fish often
increase greatly after several years of biomanipulation
(Mehner et al., 1996). As these small fish have higher
biomass-specific food requirements and occur in high
densities, their predation impact on zooplankton is
higher than that of the same biomass of adult
planktivorous fish (Romare & Bergman, 1999). The
strong predation impact is particularly detrimental for
water quality during the summer months (Romare,
Bergman & Hansson, 1999). It has been hypothesised,
in particular, that feeding by YOY fish may cause the
commonly observed phenomenon of midsummer
decline in Daphnia abundance, which is often accompanied by reduced water transparency resulting from
high phytoplankton biomass, although quantitative
evidence for this mechanism is limited (Luecke et al.,
1990; Mehner et al., 1998). Quantitative impacts of
YOY fish on zooplankton may have rarely been
demonstrated because trophic interactions between
YOY fish and zooplankton also depend on size
relationships: Fish are gape-limited and thus ingest

smaller daphnids after hatching than during later

growth stages (Schael, Rudstam & Post, 1991). However, strong demographic effects in Daphnia populations would only occur when fish feed preferentially
on mature, egg-bearing daphnids (Mehner, 2000). In
addition, it is likely that the midsummer decline of
daphnids is caused by many interacting mechanisms,
including predation by (young) fish and predatory
invertebrates as well as natural senescence and death
(Benndorf et al., 2001; Hulsmann & Voigt, 2002).
Another mechanism relating to the size-structure of
fish communities is the interaction between piscivores
and their prey. If prey fish can grow to a sufficiently
large size, they reach a refuge against being fed by
predators (Hambright, 1994; Persson & Eklov, 1995),
because strong predation may shift the age structure
of prey populations towards larger individuals
(Bronmark et al., 1995), preventing the top-down
control of large planktivores by piscivores (Lammens,
1999). As a result, planktivorous species such as
common bream or roach can be preyed upon only at
younger stages.
The shift from edible to inedible phytoplankton
species observed during biomanipulation in response
to intense grazing by daphnids is another negative
feedback mechanism in foodwebs relating to sizestructure. To overcome this problem, stocking lakes
with fish such as silver carp [Hypophthalmichthys
molitrix (Val.)], which are capable of feeding on
phytoplankton, has been suggested (Starling et al.,
1998). However, as these fish also suppress daphnids,
their stocking is recommended only in geographical
regions where daphnids are naturally absent (Radke
& Kahl, 2002).

The role of temporal variability and spatial heterogeneity

in food webs
The differing temporal or spatial scales on which most
trophic interactions in lakes occur have received
relatively little attention. The intensity of fish
zooplankton interactions may vary along spatial gradients in lakes (George & Winfield, 2000). The potential
growth rate of piscivores depends on the spatial
distribution of their prey fish (Mason & Brandt, 1996).
The predation impact by piscivorous perch and pikeperch on their own YOY descendants varied between
littoral and pelagic areas (Dorner, Wagner & Benndorf,
1999), and planktivorous YOY fish influenced daph
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Biomanipulation today summary and review

nids more strongly in littoral than in pelagic areas in
the stratified hypertrophic Bautzen Reservoir
(Hulsmann et al., 1999). A structural difference of the
trophic cascade within and outside of submerged
macrophytes stands has been found in shallow lakes,
resulting in a higher water transparency within macrophyte beds (Schriver et al., 1995). However, it is not
clear whether mechanisms acting strongly in one
particular habitat have a significant impact on the
strength of interactions at the whole-lake scale.
Planktivorous fish seeking daytime shelter from
predation by piscivorous fish or birds either in the
deep hypolimnion or in littoral vegetation may lead to
a reduction of predatory losses in pelagic zooplankton
(Gliwicz & Dawidowicz, 2001). Consequently, stocking with visually oriented pelagic piscivores such as
the strongly day-active perch (Jacobsen et al., 2002)
might induce a behaviourally mediated biomanipulation effect by preventing the daytime feeding of
planktivores on daphnids in the open water. A similar
effect can be obtained by adding fish kairomones to
the water (Gliwicz, 2002). In addition, planktivory can
be further suppressed by the presence of pelagic
predators such as pikeperch, which are active over the
whole diurnal cycle (Brabrand & Faafeng, 1993;
Holker et al., 2002).
A similar spatial coupling occurs if fish feed in one
area of a lake and excrete in another area. In this
way, fish may subsidise the pelagic nutrient pool by
feeding in nearshore areas and then migrating to the
central open-water region (littoral-pelagic coupling)
or by feeding at the lake bottom and subsequently
moving upwards into the water column (benthicpelagic coupling). In both cases, new nutrients are
supplied to pelagic phytoplankton in a directly
usable form. Restriction of this fish-mediated nutrient
transfer in some cases was found to be more
important for the success of biomanipulation than
the release of feeding pressure on zooplankton
following removal of planktivorous fish (Horppila
et al., 1998).
Consideration of habitat diversity is important
also if the physical or chemical characteristics of a
water body create spatial refuges that affect the
strength of trophic interactions. For example, layers
with reduced oxygen concentrations may help daphnids escape fish predation because fish often avoid
these zones (Wright & Shapiro, 1990; Jeppesen et al.,
1997). However, if the anoxic hypolimnion is inhab
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2459

ited by invertebrate predators such as Chaoborus,

Daphnia may be squeezed and threatened by
predation from both vertebrates in the epilimnion
and invertebrates in the hypolimnion. Dawidowicz
et al. (2002) concluded that this dual predation
pressure may have been responsible for the extinction of the large Daphnia hyalina Leydig during
biomanipulation of the deep Lake Mutek in Poland,
whereas smaller cladocerans responded positively to
the declining fish abundance.
Temporal scales are also important to consider,
because generation times of different members of
pelagic food webs differ widely (Ramcharan et al.,
1995). Life spans may range from days for phytoplankton to > 20 years for piscivorous fish. In Lake
Mendota, U.S.A., the impacts of a massive natural dieoff of a strong cisco (Coregonus artedi Lesueur) year
class on plankton community structure and water
clarity were detectable for a decade (Lathrop et al.,
2002). Yodzis (1988) suggested that evaluation of the
long-term dynamics of whole-lake experiments has to
consider time scales twice the sum of the life spans of
all members of the trophic chain, that is at least
50 years in most lakes. Such long observations following biomanipulation experiments have not yet
been made. Coupling of the dynamics of organisms
differing greatly in regard to generation times may be
apparent only over longer time scales, not over a few
months or seasons (Persson et al., 1992).
Time scale considerations also relate to the issue of
trophic level control by either predation or resource
limitation. Gliwicz (2002) pointed out that only the
bottom-up control is mediated by time-dependent
parameters such as the individual growth rate, the
reproduction rate, and the population growth rate.
Top-down control, in contrast, acts on state variables
such as biomass, individual body size, and population
density, independent of the rate at which these
entities are produced.
Consideration of temporal scales was found to be
crucial also for understanding the initiation of the
midsummer decline of daphnids, where the relative
timing of all processes involved (predation, food
supply, ageing) determines whether the decline in
Daphnia density at the end of spring eventually
results in a longer or shorter period in midsummer
with extremely low Daphnia abundance (Post &
Kitchell, 1997; Benndorf et al., 2001; Hulsmann &
Voigt, 2002).

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T. Mehner et al.

The relative proportion of piscivores

and planktivores benthivores in the fish community
As biomanipulation requires drastic removal of
planktivorous fish, the question may arise why not
create a fish community composed of piscivores only?
Intentional changes of both the piscivorous and
planktivorous levels in a whole-lake biomanipulation
experiment have indicated that the goal of removing
the planktivorous level from a lake totally may be
impossible to achieve in practice (Wissel et al., 2000).
Moreover, total removal of planktivorous fish would
leave the planktivore niche unoccupied, allowing
other groups that prey on daphnids, such as predatory invertebrates (Wissel et al., 2000), to invade and
fill the gap.
If planktivorous fish cannot and should not be
completely removed from biomanipulated lakes, what
is the most appropriate balance between planktivores
and piscivores? Besides the generally desired high
species diversity and length variability of the piscivore stock (Benndorf, 1990; Perrow et al., 1997),
Benndorf & Kamjunke (1999) recommended a proportion of 3040% piscivores. This recommendation is
based on experimental evidence from long-term biomanipulations in German lakes showing that biomanipulation is successful when the fish community
consists of >2025% (Feldberger Haussee; Wysujack
& Mehner, 2002) and up to 50% piscivores (Bautzen
Reservoir; J. Benndorf & H. Dorner, unpublished
data). Detailed energetic balances supporting these
empirical values are currently lacking, however.

The requirement of long-term maintenance

of biomanipulation measures
Biomanipulation probably does not lead to stable food
web configurations and therefore requires continuous
efforts to suppress planktivores (Kitchell, 1992;
McQueen, 1998). For example, the increased recruitment success of planktivores following a period of
planktivorous fish removals, requires control by either
piscivores or repeated manual removal (Romare &
Bergman, 1999; Van de Bund & Van Donk, 2002).
Moreover, planktivorous fish may rapidly invade
biomanipulated lakes, particularly if the lakes are
connected to other water bodies. Prevention of immigration may be especially complicated if the connections are used for navigation (Perrow et al., 1997).

Even repeated stocking of piscivores may not be

sufficient without manual removal of planktivores.
Biomanipulation by piscivore stocking had the lowest
success rate among a range of measures evaluated by
Drenner & Hambright (1999). Similarly, in the
stratified Feldberger Haussee, the continuous removal
of planktivores by low-intensity fishing did not result
in a long-term decline of the planktivorous fish stock
and did not greatly enhance crustacean biomass
(Kasprzak et al., 1993; Mehner et al., 2001). In contrast,
drastic and fast removal of > 75% of the planktivores
within one season (Meijer et al., 1999) has been
recommended as a measure to shift shallow lakes to
the clear-water state (Hansson et al., 1998). Some
critical (Barthelmes, 1988) or optimal (Benndorf,
1990) absolute densities of planktivorous fish may be
an even better endpoint for fish reductions than the
relative removal rates suggested by Meijer et al. (1999)
and others. It is not yet clear, however, whether such
critical fish densities are lake-specific or can be
generally defined. Given that even shallow lakes
may show little sign of long-term stability of biomanipulation effects (Perrow et al., 1999), repeated fish
stock reductions have been proposed as a simple and
cost-effective management strategy as long as external
nutrient supplies have not been markedly reduced
(Van De Bund & Van Donk, 2002).
The drastic reductions in planktivore fish stocks
normally required for successful biomanipulation
indicate that press perturbations are required to shift
a system into another state; the impact of pulsed
perturbations appears to be too small (Persson et al.,
1993). This conclusion may hold particularly true if
alternative stable states of food web configurations
exist, as has been proposed for shallow lakes
(Scheffer, 1998). However, there is no evidence at
present that alternative stable states also occur in
stratified lakes (Persson, 1994; Benndorf et al., 2002),
indicating that only repeated press perturbations may
hold stratified lakes in the desired food-web structure.

The management and sustainability aspects

of biomanipulation
Biomanipulation is used to improve the water quality
of lakes, and many of the studies documented in
literature were initiated because of the practical
requirement of lake restoration rather than scientific
interest (Carpenter & Kitchell, 1992). Therefore, in

2002 Blackwell Science Ltd, Freshwater Biology, 47, 24532465

Biomanipulation today summary and review

many biomanipulations, the co-operation of lake and
fishery managers, anglers and scientists was part of
the planning and manipulation phases (e.g. Benndorf,
1990; Kitchell, 1992; Lathrop et al., 2002). In addition,
success was often reported in those cases where
authorities and lake users supported the biomanipulation (Horppila et al., 1998; Perrow et al., 1999).
Guidelines for biomanipulating lakes have been
developed (Moss, Madgwick & Phillips, 1996;
Benndorf & Kamjunke, 1999) and the combination of
water quality management and sustainable fisheries
management by biomanipulation has received
increasing attention during the last years (Lammens,
1999; Wysujack et al., 2001), particularly in North
America and parts of Europe where fisheries favour
piscivorous species as catch. For example, in Lake
Mendota, U.S.A., size and bag limits imposed on
recreational fishermen were one of the most important
restrictions to support biomanipulation, which in turn
enabled the anglers to catch larger specimens than
before (Lathrop et al., 2002). In addition, during recent
years, increasing interest in catching living bream for
stocking of angling waters allows Dutch fishermen to
obtain income by combining the desired decline in
bream stocks with the effect of enhanced water
transparency (Lammens et al., 2002). Even in tropical
countries there is potential to support water-quality
goals by stocking with piscivores and controlled
fishery. Evidence from a reservoir in tropical Brazil
suggests that dense populations of omnivorous tilapias increase nutrient concentrations and promote
algal blooms as a result of P-recycling and bioturbation. Therefore, a professional tilapia cast-net fishery
has been established to control the population density
of fish and thus limit the occurrence of cyanobacterial
blooms and fish kills, in addition to generating income
for the local fishermen (Starling et al., 2002).

Conclusion
A generally better understanding of the complexity of
lake food webs and the frequent application of
biomanipulation as a lake restoration technique have
emerged from the recent developments in biomanipulation research, as compared with the findings until
1989 (Table 1). The main progress can be summarised
as follows:
1. Interactions between piscivorous, planktivorous
and benthivorous fish and their respective prey

2002 Blackwell Science Ltd, Freshwater Biology, 47, 24532465

2461

groups play a central role in biomanipulation. The

scientific data and expertise obtained in biomanipulation experiments in a range of lake types serve as
the basis for designing appropriate fish manipulation
measures in particular water bodies, and for finetuning ongoing biomanipulations. In contrast to the
situation 1015 years ago, quantitative approaches to
assess the top-down and bottom-up effects of fish are
increasingly used (bioenergetics, individual-based
modelling). The importance of young-of-the-year
fish, often neglected in earlier studies, is now fully
acknowledged as these fish are the dominant
zooplankton feeders in many lakes.
2. The confounding role of nutrients in determining
the potential for successful biomanipulations is now
clearer. The thresholds for nutrient supply and concentrations in lakes suggested in earlier studies have
been confirmed by, and more precisely described in,
recent studies. In combination with conclusion 1, this
affirmation is a partial revival of the top-down : bottom-up concept by McQueen et al. (1986), which
predicts the strongest effect of biomanipulation on
pelagic food webs when both fish and nutrients are
altered.
3. The scientific background of biomanipulation,
lake food-web ecology, has become even more
complex than was conceived after the 1989 conference. The consideration of scales is important for
understanding trophic interactions along the temporal (diel, seasonal, interannual), spatial (habitat
coupling, lake and catchment relationships), and
interorganismic (size structure, ontogeny) axes.
Besides scales, boundary conditions such as lake
depth, underwater light climate, temperature
regime, mixing intensity and trophic state govern
the response of complex food webs to changes in
predation strength. Thus, simple food-chain models
cannot be realistically assumed to reflect the multitude of possible effects of biomanipulations,
although they can mirror major food-web changes
in response to press perturbations. However, for the
fine-tuning of ongoing and for predicting success of
future biomanipulations, detailed insights into the
trophic interactions within pelagic food webs are
necessary.
4. Biomanipulation can be regarded as an approach
to water quality improvement that requires the
combination of research and management. Most lake
managers currently learn by doing, using biomanip-

2462

T. Mehner et al.

ulation as an adaptive management strategy. There is

some agreement between fisheries and water quality
management with respect to the goals of biomanipulation and ways to achieve these goals. Therefore,
even if biomanipulation ends up as a failure in some
water bodies, advantages for some lake users may
ensue. Furthermore, sound scientific knowledge on
the behaviour of aquatic ecosystems can only be
obtained by manipulating systems of adequate size
over long periods (e.g. Carpenter, 1996). As this type
of research is not easily funded in most countries, the
results from public lake management programmes
can help collecting the necessary data.

Acknowledgments
We are grateful to E. van Donk, R. Drenner, L.-A.
Hansson, E. Jeppesen, L. Persson, L.G. Rudstam, M.
Gessner, and an anonymous referee for constructive
suggestions.

References
Attayde J.L. & Hansson L.-A. (2001) The relative
importance of fish predation and excretion effects on
planktonic communities. Limnology and Oceanography,
46, 10011012.
Barko J.W. & Smart R.M. (1981) Sediment-based nutrition
of submersed macrophytes. Aquatic Botany, 10, 339352.
Barthelmes D. (1988) Fish predation and resource reaction: biomanipulation background data from fisheries
research. Limnologica, 19, 5159.
Beeck P., Tauber S., Kiel S. & Borcherding J. (2002) 0+
perch predation on 0+ bream: a case study in a
eutrophic gravel pit lake. Freshwater Biology, 47, 2359
2369.
Benndorf J. (1987) Food web manipulation without
nutrient control: a useful strategy in lake restoration?
Schweizerische Zeitschrift fur Hydrologie, 49, 237248.
Benndorf J. (1990) Conditions for effective biomanipulation; conclusions derived from whole-lake experiments
in Europe. Hydrobiologia, 200 201, 187203.
Benndorf J., Boing W., Koop J. & Neubauer I. (2002) Topdown control of phytoplankton: the role of time scale,
lake depth and trophic state. Freshwater Biology, 47,
22822295.
Benndorf J. & Kamjunke N. (1999) Anwenderrichtlinie
Biomanipulation am Beispiel der Talsperre Bautzen.
Sachsisches Landesamt fur Umwelt und Geologie, 19 pp.
Eigenverlag, Dresden.

Benndorf J., Kranich J., Mehner T. & Wagner A. (2001)

Temperature impact on the midsummer decline
of Daphnia galeata: an analysis of long-term data from
the biomanipulated Bautzen Reservoir (Germany).
Freshwater Biology, 46, 199211.
Brabrand A. & Faafeng B. (1993) Habitat shift in roach
(Rutilus rutilus) induced by pikeperch (Stizostedion
lucioperca) introduction: predation risk versus pelagic
behaviour. Oecologia, 95, 3846.
Brabrand A., Faafeng B.A. & Nilssen J.P.M. (1990)
Relative importance of phosphorus supply to phytoplankton production: fish excretion versus external
loading. Canadian Journal of Fisheries and Aquatic
Sciences, 47, 364372.
Breukelaar A.W., Lammens E.H.R.R., Breteler J.G.P.K. &
Tatrai I. (1994) Effects of benthivorous bream (Abramis
brama) and carp (Cyprinus carpio) on sediment resuspension and concentrations of nutrients and chlorophyll a. Freshwater Biology, 32, 113121.
Bronmark C., Paszkowski C.A., Tonn W.M. & Hargeby
A. (1995) Predation as a determinant of size structure
in populations of crucian carp (Carassius carassius) and
tench (Tinca tinca). Ecology of Freshwater Fish, 4, 8592.
Carney H.J. (1990) A general hypothesis for the strength
of food web interactions in relation to trophic state.
Verhandlungen der Internationalen Vereinigung fur Limnologie, 24, 487492.
Carpenter S.R. (1996) Microcosm experiments have
limited relevance for community and ecosystem ecology. Ecology, 77, 677680.
Carpenter S.R., Cole J.J., Hodgson J.R., Kitchell J.F., Pace
M.L., Bade D., Cottingham K.L., Essington T.E.,
Houser J.N. & Schindler D.E. (2001) Trophic cascades,
nutrients, and lake productivity: whole-lake experiments. Ecological Monographs, 71, 163186.
Carpenter S.R. & Kitchell J.F. (1992) Trophic cascade and
biomanipulation: interface of research and management a reply to the comment by DeMelo et al.
Limnology and Oceanography, 37, 208213.
Carpenter S.R., Kitchell J.F. & Hodgson J.R. (1985)
Cascading trophic interactions and lake productivity.
Bioscience, 35, 634639.
Dawidowicz P., Prejs A., Engelmayer A., Martyniak A.,
Kozlowski J., Kufel L. & Paradowska M. (2002)
Hypolimnetic anoxia hampers top-down food-web
manipulation in a eutrophic lake. Freshwater Biology
47, 24012409.
Declerck S., DeMeester L., De Smedt P., Rommens W.,
Vyverman W., Geenens V., Van Wichelen J., Degans H.
& Decleer K. (2000) Clear water and charophytes in a
hypertrophic pond. Verhandlungen der Internationalen
Vereinigung fur Limnologie, 27, 541.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 24532465

Biomanipulation today summary and review

Dorner H., Wagner A. & Benndorf J. (1999) Predation by
piscivorous fish on age-0 fish: spatial and temporal
variability in a biomanipulated lake (Bautzen reservoir, Germany). Hydrobiologia, 408 409, 3946.
Drenner R.W. & Hambright K.D. (1999) Biomanipulation
of fish assemblages as a lake restoration technique.
Archiv fur Hydrobiologie, 146, 129165.
Elser J.J. & Goldman C.R. (1991) Zooplankton effects on
phytoplankton in lakes of contrasting trophic status.
Limnology and Oceanography, 36, 6490.
George D.G. & Winfield I.J. (2000) Factors influencing the
spatial distribution of zooplankton and fish in Loch
Ness, UK. Freshwater Biology, 43, 557570.
Gliwicz Z.M. (2002) On the different nature of top-down
and bottom-up effects in pelagic food webs. Freshwater
Biology, 47, 22962312.
Gliwicz Z.M. & Dawidowicz P. (2001) Roach habitat
shifts and foraging modified by alarm substance. 1.
Field evidence. Archiv fur Hydrobiologie, 150, 357376.
Grimm M.P. & Backx J. (1990) The restoration of shallow
eutrophic lakes and the role of northern pike, aquatic
vegetation and nutrient concentration. Hydrobiologia,
200 201, 557566.
Gulati R.D., Lammens E.H.R.R., Meijer M.-L. & Van
Donk E. (Eds) (1990) Biomanipulation Tool for Water
Management. Kluwer, Dordrecht.
Hairston N.G., Smith F.E. & Slobodkin L.B. (1960)
Community structure, population control, and competition. The American Naturalist, 94, 421425.
Hambright D. (1994) Morphological constraints in the
piscivoreplanktivore interaction: implications for the
trophic cascade hypothesis. Limnology and Oceanography,
39, 897912.
Hansson L.-A., Annadotter H., Bergman E., Hamrin S.F.,
Jeppesen E., Kairesalo T., Luokkanen E., Nilsso P.-A.,
Sndergaard M. & Strand J. (1998) Biomanipulation as
an application of food-chain theory: constraints,
synthesis, and recommendations for temperate lakes.
Ecosystems, 1, 558574.
Holker F., Haertel S.S., Steiner S. & Mehner T. (2002)
Effects of piscivore-mediated habitat use on growth,
diet and zooplankton consumption of roach: an individual-based modelling approach. Freshwater Biology,
47, 23452358.
Horppila J., Peltonen H., Malinen T., Luokkanen E. &
Kairesalo T. (1998) Top-down or bottom-up effects by
fish: issues of concern in biomanipulation of lakes.
Restoration Ecology, 6, 2028.
Hulsmann S., Mehner T., Worischka S. & Plewa M. (1999)
Is the difference in population dynamics of Daphnia
galeata in littoral and pelagic areas of a long-term
biomanipulated reservoir affected by age-0 fish predation? Hydrobiologia, 408 409, 5763.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 24532465

2463

Hulsmann S. & Voigt. H. (2002) Life history of Daphnia

galeata in a hypertrophic reservoir and consequences of
non-consumptive mortality for the initiation of a
midsummer decline. Freshwater Biology, 47, 2313
2324.
Jacobsen L., Berg S., Broberg M., Jepsen N. & Skov C.
(2002) Activity and food choice of piscivorous perch
(Perca fluviatilis) in a eutrophic shallow lake: a radiotelemetry study. Freshwater Biology, 47, 23702379.
Jeppesen E., Jensen J.P., Sondergaard M., Lauridsen T.,
Pedersen L.J. & Jensen L. (1997) Top-down control in
freshwater lakes: the role of nutrient state, submerged
macrophytes and water depth. Hydrobiologia, 342 343,
151164.
Jeppesen E., Kristensen P., Jensen J.P., Sondergaard M.,
Mortensen E. & Lauridsen T. (1991) Recovery resilience following a reduction in external phosphorus
loading of shallow, eutrophic Danish lakes: duration,
regulating factors and methods for overcoming resilience. Memorie Dell Istituto Italiano Di Idrobiologia Dott.
Marco de Marchi, 48, 127148.
Kasprzak P., Krienitz L. & Koschel R. (1993) Biomanipulation: a limnological in-lake ecotechnology of eutrophication management? Memorie Dell Istituto Italiano Di
Idrobiologia Dott. Marco de Marchi, 52, 151169.
Kitchell J.F. (Ed.) (1992) Food Web Management, A Case
Study of Lake Mendota, pp. 553. Springer, New York.
Koschel R. (1997) Structure and function of pelagic calcite
precipitation in lake ecosystems. Verhandlungen der
Internationalen Vereinigung fur Limnologie, 26, 343349.
Lammens E.H.R.R. (1999) The central role of fish in lake
restoration and management. Hydrobiologia, 395 396,
191198.
Lammens E.H.R.R., Gulati R.D., Meijer M.-L. & Van
Donk E. (1990) The first biomanipulation conference: a
synthesis. Hydrobiologia, 200 201, 619627.
Lammens E.H.R.R., Van Nes E.H. & Mooij W.M. (2002)
Differences in the exploitation of bream in three
shallow lake systems and their relation to water
quality. Freshwater Biology, 47, 24352442.
Lathrop R.C., Johnson B.M., Johnson T.B., Vogelsang
M.T., Carpenter S.R., Hrabic T.R., Kitchell J.F., Magnuson J.J., Rudstam L.G. & Stewart R.S. (2002)
Stocking piscivores to improve fishing and water
clarity: a synthesis of the Lake Mendota biomanipulation project. Freshwater Biology, 47, 24102424.
Luecke C., Vanni M.J., Magnuson J.J., Kitchell J.F. &
Jacobson P.T. (1990) Seasonal regulation of Daphnia
populations by planktivorous fish: implications for the
spring clear-water phase. Limnology and Oceanography,
35, 17181733.
Mason D.M. & Brandt S.B. (1996) Effect of spatial scale
and foraging efficiency on the predictions made by

2464

T. Mehner et al.

spatially-explicit models of fish growth rate potential.

Environmental Biology of Fishes, 45, 283298.
McQueen D.J. (1998) Freshwater food web manipulation:
a powerful tool for water quality improvement, but
maintenance is required. Lakes and Reservoirs: Research
and Management, 3, 8394.
McQueen D.J., Post J.R. & Mills E.L. (1986) Trophic
relationships in freshwater pelagic ecosystems. Canadian Journal of Fisheries and Aquatic Sciences, 43, 1571
1581.
Mehner T. (2000) Influence of spring water warming on
predation rate of underyearling fish on Daphnia a
deterministic simulation approach. Freshwater Biology,
45, 253263.
Mehner T., Hulsmann S., Worischka S., Plewa M. &
Benndorf J. (1998) Is the midsummer decline of Daphnia
really induced by age-0 fish predation? Comparison of
age-0 fish consumption and Daphnia mortality and life
history parameters in a biomanipulated reservoir.
Journal of Plankton Research, 20, 17971811.
Mehner T., Kasprzak P., Wysujack K., Laude U. &
Koschel R. (2001) Restoration of a stratified lake
(Feldberger Hausee, Germany) by a combination of
nutrient load reduction and long-term biomanipulation. International Review of Hydrobiology, 86, 253265.
Mehner T., Schultz H., Werner M.-G., Wieland F., Herbst
R. & Benndorf J. (1996) Do 0+ percids couple the
trophic cascade between fish and zooplankton in the
top-down manipulated Bautzen reservoir (Germany)?
Publicaciones Especiales Del Instituto Espanol de Oceanografia, 21, 243251.
Meijer M.-L., De Boois I., Scheffer M., Portielje R. &
Hosper H. (1999) Biomanipulation in shallow lakes in
the Netherlands: an evaluation of 18 case studies.
Hydrobiologia, 408 409, 1330.
Moss B., Madgwick J. & Phillips G. (1996) A Guide to the
Restoration of Nutrient-Enriched Shallow Lakes, pp. 179,
Broads Authority, Norwich.
Perrow M.R., Jowitt A.J.D., Leigh S.A.C., Hindes A.M. &
Rhodes J.D. (1999) The stability of fish communites in
shallow lakes undergoing restoration: expectations
and experiences from the Norfolk Broads (U.K.).
Hydrobiologia, 408 409, 85100.
Perrow M.R., Meijer M.-L., Dawidowicz P. & Coops H.
(1997) Biomanipulation in shallow lakes: state of the
art. Hydrobiologia, 342 343, 355365.
Persson L. (1994) Natural shifts in the structure of fish
communities: mechanisms and constraints on pertubation sustenance. In: Rehabilitation of Freshwater Fisheries (Ed. I.G. Cowx), pp. 421434. Fishing News Books,
Oxford.
Persson L., Andersson G., Hamrin S.F. & Johansson L.
(1988) Predator regulation and primary production

along the productivity gradient of temperate lake

ecosystems. In: Complex Interactions in Lake Communities
(Ed. S.R. Carpenter), pp. 4565. Springer, New York.
Persson L., Bystrom P. & Wahlstrom E. (2000) Cannibalism and competition in Eurasian perch: population
dynamics of an ontogenetic omnivore. Ecology, 81,
10581071.
Persson L., Diehl S., Johansson L., Andersson G. &
Hamrin S. (1992) Trophic interactions in temperate
lake ecosystems: a test of food chain theory. The
American Naturalist, 140, 5984.
Persson L. & Eklov P. (1995) Prey refuges affecting
interactions between piscivorous perch and juvenile
perch and roach. Ecology, 76, 7081.
Persson L., Johansson L., Andersson G., Diehl S. &
Hamrin S.F. (1993) Density dependent interactions in
lake ecocsystems: whole lake perturbation experiments. Oikos, 66, 193208.
Post D.M. & Kitchell J.F. (1997) Trophic ontogeny and life
history effects on interactions between age-0 fishes and
zooplankton. Archiv fur Hydrobiologie Special Issues
Advances in Limnology, 49, 112.
Radke R.J. & Kahl U. (2002) Effects of a filter-feeding fish
[silver carp. Hypophthalmichthys molitrix (Val.)] on the
structure of phytoplankton and zooplankton in a
mesotrophic lake: results from an enclosure experiment. Freshwater Biology, 47, 23372344.
Ramcharan C.W., McQueen D.J., Demers E., Popiel S.A.,
Rocchi A.M., Yan N.D., Wong A.H. & Hughes K.D.
(1995) A comparative approach to determining the role
of fish predation in structuring limnetic ecosystems.
Archiv fur Hydrobiologie, 133, 389416.
Romare P. & Bergman E. (1999) Juvenile fish expansion
following biomanipulation and the resulting effect on
the predation pressure on zooplankton. Hydrobiologia,
404, 8997.
Romare P., Bergman E. & Hansson L.-A. (1999) The
impact of larval and juvenile fish on zooplankton and
algal dynamics. Limnology and Oceanography, 44, 1655
1666.
Sarnelle O. (1992) Nutrient enrichment and grazer effects
on phytoplankton in lakes. Ecology, 73, 551560.
Schael D.M., Rudstam L.G. & Post J.R. (1991) Gape limitation and prey selection in larval yellow perch (Perca
flavescens), freshwater drum (Aplodinotus grunniens), and
black crappie (Pomoxis nigromaculatus). Canadian Journal
of Fisheries and Aquatic Sciences, 48, 191925.
Scheffer M. (1998) Ecology of Shallow Lakes. Chapman &
Hall, London.
Schindler D.E., Kitchell J.F., He X., Carpenter S.R.,
Hodgson J.R. & Cottingham K.L. (1993) Food web
structure and phosphorus cycling in lakes. Transactions
of the American Fisheries Society, 122, 756772.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 24532465

Biomanipulation today summary and review

Schriver P., Bgestrand J., Jeppesen E. & Sndergaard M.
(1995) Impact of submerged macrophytes on fishzooplanktonphytoplankton interactions: large-scale
enclosure experiments in a shallow lake. Freshwater
Biology, 33, 255270.
Shapiro J., Lamarra V. & Lynch M. (1975) Biomanipulation: an ecological approach to lake restoration. In:
Water Quality Management Through Biological Control
(Eds P.L. Brezonik & J.L. Fox), pp. 8596. University of
Florida, Gainesville.
Skov C., Perrow M.R., Berg S. & Skovgaard H. (2002)
Changes in the fish community and water quality
during seven years of stocking piscivorous fish in a
shallow lake. Freshwater Biology, 47, 23882400.
Sndergaard M., Jensen J.P. & Jeppesen E. (2001)
Retention and internal loading of phosphorus in
shallow eutrophic lakes. The Scientific World, 1, 427442.
Stansfield J.H., Perrow M.R., Tench L.D., Jowitt A.J.D. &
Taylor A.A.L. (1997) Submerged macrophytes as
refuges for grazing Cladocera against fish predation:
observations on seasonal changes in relation to
macrophyte cover and predation pressure. Hydrobiologia,
342 343, 229240.
Starling F., Beveridge M., Lazzaro X. & Baird D. (1998)
Silver carp biomass effects on the plankton community
in Paranoa resevoir (Brazil) and an assessment of its
potential for improving water quality in lacustrine
environments. International Review of Hydrobiology, 83,
499507.
Starling F., Lazzaro X., Cavalcanti C. & Moreira R. (2002)
Contribution of omnivorous tilapia to eutrophication
of a shallow tropical reservoir: evidence from a fish
kill. Freshwater Biology, 47, 24432452.
Svensson J.M., Bergman E. & Andersson G. (1999) Impact
of cyprinid reduction on the benthic macroinvertebrate
community and implications for increased nitrogen
retention. Hydrobiologia, 404, 99112.
Tarvainen M., Sarvala J. & Helminen H. (2002) The role
of phosphorus release by roach [Rutilus rutilus (L.)] in
the water quality changes of a biomanipulated lake.
Freshwater Biology, 47, 23252336.
Tatrai I. & Istvanovics V. (1986) The role of fish in the
regulation of nutrient cycling in Lake Balaton. Freshwater Biology, 16, 417424.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 24532465

2465

Van de Bund W.J. & Van Donk E. (2002) Short-term and

long-term effects of zooplanktivorous fish removal in a
shallow lake: a synthesis of 15 years of data from Lake
Zwemlust. Freshwater Biology, 47, 23802387.
Van Donk E., Grimm M.P., Gulati R.D. & Klein Breteler
J.P.G. (1990) Whole-lake food-web manipulation as a
means to study community interactions in a small
ecosystem. Hydrobiologia, 200 201, 275289.
Van Donk E., Gulati R.D., Iedema A. & Meulemans J.
(1993) Macrophyte-released shifts in the nitrogen and
phosphorus contents of the different trophic levels in a
biomanipulated shallow lake. Hydrobiologia, 251, 1926.
Werner E.E. (1992) Individual behavior and higher-order
species interactions. The American Naturalist, 140 (Suppl.), S5S32.
Werner E.E. & Gilliam J.F. (1984) The ontogenetic niche
and species interactions in size-structured populations.
Annual Review of Ecology and Systematics, 15, 393425.
Winfield I.J. (1986) The influence of simulated aquatic
macrophytes on the zooplankton consumption rate of
juvenile roach, Rutilus rutilus, rudd, Scardinius erythrophthalmus, and perch, Perca fluviatilis. Journal of Fish
Biology, 29 (Suppl. A), 3748.
Wissel B., Freier K., Muller B., Koop J. & Benndorf J.
(2000) Moderate planktivorous fish biomass stabilizes
biomanipulation by suppressing large invertebrate predators of Daphnia. Archiv fur Hydrobiologie, 149, 177192.
Wright D. & Shapiro J. (1990) Refuge availability: a key to
understanding the summer disappearance of Daphnia.
Freshwater Biology, 24, 4362.
Wysujack K., Laude U., Anwand K. & Mehner T. (2001)
Stocking, population development and food composition of pike Esox lucius in the biomanipulated
Feldberger Haussee (Germany) implications for
fisheries management. Limnologica, 31, 4551.
Wysujack K. & Mehner T. (2002) Comparison of losses of
planktivorous fish by predation and seine-fishing in a
lake undergoing long-term biomanipulation. Freshwater Biology, 47, 24252434.
Yodzis P. (1988) The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology, 69, 508515.
(Manuscript accepted 15 April 2002)