Freshwater Biology (2002) 47, 2282–2295
Top-down control of phytoplankton: the role of time
scale, lake depth and trophic state
J Ü R G E N B E N N D O R F , W I E B K E B Ö I N G , * J O C H E N K O O P and I V O N N E N E U B A U E R
Institute of Hydrobiology, Dresden University of Technology, Mommsenstr. 13, D-01062 Dresden, Germany
*Present address: Department of Biological Sciences, Louisiana State University, Baton Rouge 70803 LA, U.S.A.
SU M M A R Y
1. One of the most controversial issues in biomanipulation research relates to the
conditions required for top-down control to cascade down from piscivorous fish to
phytoplankton. Numerous experiments have demonstrated that Phytoplankton biomass
Top-Down Control (PTDC) occurs under the following conditions: (i) in short-term
experiments, (ii) shallow lakes with macrophytes, and (iii) deep lakes of slightly eutrophic
or mesotrophic state. Other experiments indicate that PTDC is unlikely in (iv) eutrophic or
hypertrophic deep lakes unless severe light limitation occurs, and (v) all lakes characterised by extreme nutrient limitation (oligo to ultraoligotrophic lakes).
2. Key factors responsible for PTDC under conditions (i) to (iii) are time scales preventing
the development of slow-growing inedible phytoplankton (i), shallow depth allowing
macrophytes to become dominant primary producers (ii), and biomanipulation-induced
reduction of phosphorus (P) availability for phytoplankton (iii).
3. Under conditions (iv) and (v), biomanipulation-induced reduction of P-availability
might also occur but is insufficient to alter the epilimnetic P-content enough to initiate
effective bottom-up control (P-limitation) of phytoplankton. In these cases, P-loading is
much too high (iv) or P-content in the lake much too low (v) to initiate or enhance
P-limitation of phytoplankton by a biomanipulation-induced reduction of P-availability.
However, PTDC may exceptionally result under condition (iv) if high mixing depth and ⁄ or
light attenuation cause severe light limitation of phytoplankton.
4. Recognition of the five different conditions reconciles previous seemingly contradictory
results from biomanipulation experiments and provides a sound basis for successful
application of biomanipulation as a tool for water management.
Keywords: biomanipulation, enclosures, food web manipulation, macrophytes, phosphorus, phytoplankton, water management, whole-lake experiments
Introduction
Both the biomanipulation concept (Shapiro, Lamarra
& Lynch, 1975) and the trophic cascade hypothesis
(Carpenter, Kitchell & Hodgson, 1985) are based on
the fundamental assumption that a change in predator
biomass at the highest trophic level of an aquatic food
web (piscivorous fish) cascades down to the lowest
Correspondence: Jürgen Benndorf, Institute of Hydrobiology,
Dresden University of Technology, Mommsenstr. 13, D-01062
Dresden, Germany. E-mail: [email protected]
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trophic level (phytoplankton). The competing bottomup ⁄ top-down hypothesis (McQueen, Post & Mills,
1986) predicts that top-down effects are strong at the
top of the food web and weaken towards the bottom,
because phytoplankton biomass is thought to be more
strongly controlled by resources (bottom-up) than by
grazing (top-down). In an evaluation of 33 whole-lake
biomanipulation experiments, Reynolds (1994) concluded that top-down effects at the lower trophic
levels are not the rule: 11 experiments support the
biomanipulation ⁄ trophic cascade hypothesis whereas
16 experiments support the bottom-up ⁄ top-down
2002 Blackwell Science Ltd
Top-down control of phytoplankton
hypothesis. The remaining six experiments provided
inconclusive answers. As both hypotheses were thus
refuted by a number of cases, neither can be regarded
to be generally valid. The validity of both is obviously
restricted to certain boundary conditions.
In this review, we explore the boundary conditions
required for top-down control of phytoplankton
biomass. These boundary conditions are seemingly
the same as that of the assumptions underlying the
trophic cascade hypothesis. However, it must be
emphasised that there are two quite different theoretical possibilities to achieve top-down control of
phytoplankton, namely (1) by a strong direct cascading effect on phytoplankton biomass (grazing by
zooplankton), or (2) by strong direct cascading effects
of zooplankton on phytoplankton resources rather
than on biomass. In the second case, phytoplankton
biomass is reduced by an indirect cascading effect
passing through a positive feedback (bottom-up)
between resources and phytoplankton. Possibility (1)
is consistent with the trophic cascade hypothesis (i.e.
all trophic levels down to phytoplankton and dissolved phosphate are negatively correlated), whereas
possibility (2) emerges from the bottom-up ⁄ top-down
hypothesis (i.e. higher trophic levels are negatively
correlated; lower trophic levels reveal positive correlation coefficients). However, as biomanipulation
success is mainly judged by water transparency and
phytoplankton biomass (Drenner & Hambright, 1999),
both possibilities – regardless of their attribution to the
respective hypothesis – would considerably enhance
the chance for successful application of biomanipulation as a tool in water quality management.
The main focus of this review consists in identifying the respective boundary conditions responsible
for the implementation of the two possibilities to
reduce phytoplankton by biomanipulation. Based on
comprehensive comparative studies (e.g. Reynolds,
1994; McQueen, 1998; Drenner & Hambright, 1999;
Meijer et al., 1999; Jeppesen et al., 2000) and our own
experience (e.g. Benndorf, 1987, 1990, 1995; Benndorf
et al., 2000; Wissel et al., 2000), we assume that three
conditions may be particularly important in this
context: time scale, lake depth and trophic state. The
role of these conditions in top-down control of
phytoplankton will be evaluated using case studies
carried out in five types of freshwater systems:
(i) short-term experiments in enclosures, (ii) longterm experiments in shallow lakes, (iii) long-term
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experiments in mesotrophic (or slightly eutrophic)
deep lakes, (iv) long-term experiments in eutrophic
and hypertrophic deep lakes and (v) long-term
experiments in oligotrophic deep lakes. These five
categories encompass all the important combinations
of the three above-mentioned boundary conditions.
We suppose in all cases discussed in this review a
successful enhancement of large-sized herbivorous
zooplankton by an appropriate management of the
fish community. Case studies (or periods) not fulfilling this prerequisite were excluded.
Short-term experiments in enclosures
Strong top-down effects on phytoplankton biomass
were demonstrated in numerous enclosure experiments (e.g. Elser & Goldman, 1991; Kurmayer &
Wanzenböck, 1996; Vanni & Layne, 1997; Bertolo
et al., 2000). However, because of the large difference
in scales, it is questionable whether these findings can
be transferred to whole lakes (Carpenter, 1996). In
addition to large differences in spatial scales, enclosure experiments are also unrealistically short. They
usually must be terminated after 4–6 weeks because
of excessive algal growth on the enclosure walls, even
in mesotrophic and oligotrophic lakes. Four to six
weeks are too short for phytoplankton to reach a new
‘steady-state’ fully adapted to strong top-down
effects. This is demonstrated by results from hypertrophic Bautzen Reservoir (Germany) in combination
with a concurrent enclosure experiment in a nearby
small lake (Böing et al., 1998).
Total chlorophyll a concentrations in enclosures
containing large Daphnia (Daphnia pulex Leydig,
D. rosea Leydig) were severely reduced by day 36
irrespective of the nutrient content (Fig. 1, left). On the
other hand, the proportion of inedible phytoplankton
increased from less than 10% at the beginning to
about 50% on day 36 (Fig. 1, middle-left). We do not
know whether this development towards more inedible phytoplankton would have continued had the
experiment not been terminated. If so, the low total
chlorophyll a concentration at the end of the experiment must be regarded as transient after a disturbance. Evidence for this view emerges from the
phytoplankton development during the same period
in the whole-lake biomanipulation experiment in
Bautzen Reservoir (see Benndorf & Schultz, 2000, for
experimental conditions). As soon as the filtration rate
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J. Benndorf et al.
Fig. 1 Temporal development of edible (<30 lm) and inedible (>30 lm) phytoplankton in 3.5 m3-enclosures (left, original data) and in
Bautzen Reservoir (right, source data from Böing et al., 1998) under strong Daphnia-grazing pressure. Experimental conditions of the
enclosure experiment (arithmetic mean ± 1 SD): C: control (TP ¼ 84 ± 25 lg L)1; TN ¼ 1.8 ± 0.22 mg L)1; Daphnia
spp. ¼ 0 mg wet weight L)1); N: addition of nutrients, no Daphnia (TP ¼ 853 ± 60 lg L)1; TN ¼ 11.6 ± 1.25 mg L)1; Daphnia
spp. ¼ 0 mg wet weight L)1); D: addition of Daphnia, no addition of nutrients (TP ¼ 89 ± 23 lg L)1; TN ¼ 1.92 ± 0.02 mg L)1;
Daphnia spp. ¼ 3.1 ± 0.9 mg wet weight L)1); DN: addition of Daphnia and nutrients (TP ¼ 847 ± 136 lg L)1;
TN ¼ 12.33 ± 1.56 mg L)1; Daphnia spp. ¼ 2.6 ± 0.7 mg wet weight L)1); conditions in Bautzen Reservoir: TP ¼ 142 ± 69 lg L)1;
TN ¼ 3.69 ± 0.26 mg L)1; Daphnia spp. ¼ 5.4 ± 6.6 mg wet weight L)1); TN: total inorganic nitrogen; TP: total phosphorus.
of D. galeata Sars exceeded about 0.1 L L)1 d)1 in midMay (day 0 in Fig. 1, right), both edible and inedible
phytoplankton was suppressed for about 5 weeks
(until day 36 in Fig. 1, right). The complete agreement
with enclosure results is noteworthy. Only after this
‘transient phase’ did inedible phytoplankton (mainly
Microcystis spp.) start exponential growth and reach
high biomass at the end of the clear-water phase (day
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78 in Fig. 1, right). Although the filtration rate of
daphnids fluctuated considerably during that period,
it never dropped below 0.1 L L)1 day)1 and peaked as
high as 1.1 L L)1 day)1 (see Böing et al., 1998). Thus,
the grazing pressure in enclosures and in the wholelake experiment was high and comparable during the
observation period shown in Fig. 1.
This comparison of phytoplankton development in
two systems under strong grazing pressure confirms
previous conclusions (Reynolds, 1994; Carpenter,
1996) that the short time scale of enclosure experiments prevents the development of slow-growing
large (inedible) phytoplankton which in the long-term
will fill in the niches opened by intense grazing (cf.
Gliwicz, 1975, 1990, 2002). Enclosure experiments,
therefore, tend to support the cascade theory (Fig. 2),
but their findings are largely irrelevant for whole-lake
situations (e.g. Kasprzak & Lathrop, 1997). This
conclusion, of course, does not preclude the usefulness of enclosure experiments for studying short-term
processes (e.g. Lyche et al., 1996; Vanni & Layne,
1997).
Long-term experiments in shallow lakes
There is overwhelming evidence that biomanipulation
is most successful in shallow lakes with a mean depth
Fig. 2 Schematic diagram showing changes in biomass (or P
concentration) and sign of correlations between biomass (or P
concentration) of adjacent trophic levels under strong top-down
control in short-term experiments (e.g. enclosure studies).
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295
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<3 m (Gulati et al., 1990; Reynolds, 1994; Drenner &
Hambright, 1999; Meijer et al., 1999). The main reason
is that shallow lakes may occur in two alternative
stable states, a turbid phytoplankton-dominated state
and a clear-water state characterised by dense stands
of submerged macrophytes (Moss, 1990; Blindow
et al., 1993; Perrow et al., 1997; Scheffer, 1998). The
clear-water state is more likely at low phosphorus
levels and high grazing pressure on phytoplankton
(Jeppesen et al., 1997, 2000; Meijer et al., 1999).
Enhanced grazing pressure by biomanipulation is
only critical, however, as long as dense macrophyte
stands are lacking (Persson et al., 1993; Perrow et al.,
1997; Meijer et al., 1999). Numerous studies have
indeed shown a negligible top-down control of phytoplankton under clear-water conditions (macrophyte
dominance) during summer (e.g. Meijer et al., 1999;
Blindow et al., 2000; Declerck et al., 2000). Therefore,
mechanisms other than grazing pressure must affect
phytoplankton biomass under conditions of macrophyte dominance.
Indirect bottom-up effects are likely also to play
an important role in suppressing phytoplankton
once macrophytes are established. Greater nitrogen
limitation as a result of enhanced nitrification ⁄ denitrification in the sediment (Jeppesen et al., 1998) and
competition for nitrogen between phytoplankton
and macrophytes (Declerck et al., 2000) are such
indirect effects. The release of allelopathic compounds by macrophytes might be just as important
(Declerck et al., 2000). Groß, Meyer & Schilling
(1996), for example, detected in Myriophyllum spicatum L. an algicidal polyphenol (tellimagrandin II),
which inhibited algal extracellular enzymes, including alkaline phosphatase. Inhibition of alkaline
phosphatase by macrophytes has also been observed
by Yiyong, Jianqiu & Yongqing (2000). This mechanism may explain why clear-water states are more
stable at low phosphorus concentrations: the competitive advantage of macrophytes resulting from
the inhibition of algal phosphatase is reduced (or
eliminated) when ortho-phosphate concentrations
(PO43 –P) are high.
Inedible phytoplankton usually develops sooner or
later under strong top-down control in deep lakes
without macrophytes (see above). Similar mass developments are uncommon in macrophyte-dominated
shallow lakes, even when grazing pressure is strong
(Gulati, 1995). Allelopathy and nitrogen limitation
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J. Benndorf et al.
might account for this phenomenon. However, sustained clear-water states during summer have also
been reported from shallow sewage ponds lacking
macrophytes (Uhlmann, 1955). Consequently, other
mechanisms preventing the mass development of
inedible phytoplankton under strong Daphnia grazing
in shallow waterbodies can also occur.
Thus, earlier conclusions (Gulati et al., 1990;
Reynolds, 1994; Drenner & Hambright, 1999; Meijer
et al., 1999) can be confirmed that a trophic cascade
down to the phytoplankton level is found in longterm biomanipulation experiments in shallow lakes
(Fig. 3). However, mechanisms other than top-down
effects are also involved. Bottom-up effects dominate
the trophic interactions between lower trophic levels
as demonstrated by positive correlations between
zooplankton and macrophytes abundance and
between total primary producers and phosphate
concentrations (Fig. 3). These bottom-up effects, however, are at least partly induced by top-down control.
The key factor for this is shallow depth allowing
macrophytes to become dominant (inedible) primary
producers.
Fig. 3 Schematic diagram showing changes in biomass (or P
concentration) and sign of correlations between biomass (or P
concentration) of adjacent trophic levels under strong top-down
control in long-term experiments in shallow lakes.
Long-term experiments in mesotrophic
and slightly eutrophic deep lakes
Striking differences in phytoplankton reduction by
biomanipulation in deep lakes (mean depth >5 m) are
caused by differences in phosphorus (P) loading.
Whereas eutrophic and hypertrophic lakes usually
show only a temporal reduction in phytoplankton
biomass (clear-water phase in spring or early summer,
e.g. Lampert et al., 1986; Sommer et al., 1986), strong
top-down control in deep mesotrophic to slightly
eutrophic lakes can cause sustained phytoplankton
biomass reductions (Stenson et al., 1978; Stenson,
1988; Wissel et al., 2000). The key factor for this
difference might consist in the biomanipulationinduced reduction of P-availability for phytoplankton
(Benndorf, 1992; Sterner, Elser & Hessen, 1992). The
most important mechanisms behind the reduced
P-availability are (1) enhanced vertical P-translocation
through sedimentation, or migration (Wright &
Shapiro, 1984; Andersson, Graneli & Stenson, 1988;
Bloesch & Bürgi, 1989; Mazumder et al., 1992) and (2)
P-accumulation in Daphnia biomass (Lyche et al.,
1996). These mechanisms obviously work regardless
of the phosphorus loading or concentration in all
deep lakes under strong top-down control. However,
as the BEThP hypothesis predicts (BEThP ¼ Biomanipulation Efficiency Threshold of P-loading; Benndorf, 1987), a biomanipulation-induced decrease of
epilimnetic P can be expected only if two conditions
are fulfilled: (1) total P in the epilimnion remains
sufficiently high to allow for a further decrease (see
below: oligotrophic lakes) and (2) a certain threshold
of external and internal P-loading (BEThP) is not
exceeded. Although BEThP is probably variable from
lake to lake, a comparison of biomanipulation effects
in deep lakes with quite different P-loadings resulted
in a rough estimate of 0.6–0.8 g total P m)2 year)1
(Benndorf & Miersch, 1991). Above this threshold,
biomanipulation-induced P-losses are fully compensated by exceedingly high external and ⁄ or internal
P-loading. Consequently, total in-lake P concentration
remains constantly high even under strong top-down
control. It must be emphasised that BEThP was defined
for deep lakes in terms of P-loading only and therefore
must not be confused with thresholds of P concentration in shallow lakes as proposed by Jeppesen et al.
(1990, 1997). The main requirement underlying the
BEThP concept is to achieve a negative mass balance of
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Fig. 4 Schematic representation of the BEThP hypothesis
(BEThP ¼ Biomanipulation Efficiency Threshold of P-loading;
Benndorf, 1987): a biomanipulation-induced decrease in total P
concentration reduces phytoplankton biomass; a decline in the
in-lake concentration of total P resulting from biomanipulation
occurs only if P-loading is lower than the sum of all P-losses.
total P in the epilimnion (i.e. P-losses by sedimentation into the hypolimnion and flushing > external
P-loading and import from the hypolimnion; Fig. 4).
This requirement can even be met at relatively high P
concentrations (see Fig. 5), but not when P-loading is
high. Thus, it is impossible to convert the BEThPestimate of 0.6–0.8 g total P m)2 year)1 (see above) to
concentrations of P in a lake.
Our long-term biomanipulation experiment in two
small deep quarry lakes in Gräfenhain near Dresden,
Germany (Benndorf et al., 1984, 2000; Wissel et al.,
2000), provides an example in support of the BEThP
hypothesis. The external P-loading of both lakes is
rather low (about 0.6 g P m)2 year)1, almost exclusively because of fallen leaves), and internal P-loading
has been greatly reduced by repeated sediment
treatment with nitrate according to Ripl (1976). Total
P-loading therefore is very probably below BEThP in
both lakes. Additionally, the spring P concentration
has been reduced by artificially enhancing P-precipitation with Fe2(SO4)3 (see Wissel et al., 2000). After
nitrate treatment and P-precipitation, the lakes were
in a slightly eutrophic state. One of the lakes (Pisci 2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295
Fig. 5 Cumulative frequency distributions of epilimnetic chlorophyll a, epilimnetic total P concentration and P-sedimentation
(measured in sediment traps according to Horn & Horn, 1990) in
Planktivore Lake and Piscivore Lake in Gräfenhain, Germany
(original data). Only summer values (June to August) during the
period of optimum biomanipulation in Piscivore Lake and
extremely high planktivory in Planktivore Lake are shown (1996,
1998, 1999; see Wissel et al., 2000, for experimental design).
vore Lake) was biomanipulated for many years with
moderate success (Benndorf et al., 1984, 2000). Biomanipulation was finally most efficient after an ‘optimum’ fish density had been adjusted in 1996 (Wissel
et al., 2000). The other lake (Planktivore Lake) was
permanently colonised (except in 1997) by a dense
population of a small planktivorous cyprinid, Leucaspius delineatus L. (see Benndorf et al., 2000 and
Wissel et al., 2000, for details).
Total chlorophyll a (including the inedible fraction) during summer was distinctly lower in Piscivore Lake compared with Planktivore Lake (Fig. 5,
top). In contrast to highly eutrophic or hypertrophic
lakes (see below), inedible phytoplankton was not
able to completely fill the niche opened by intensive
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J. Benndorf et al.
Daphnia grazing, not even during the entire summer period (3 months). This observation can be
explained by reduced total P concentrations in the
epilimnion of Piscivore Lake (Fig. 5, middle) which
were mainly caused by an increased P-sedimentation (Fig. 5, bottom). As the only obvious difference
between the two lakes consisted in the different
patterns of top-down control, the direct and indirect
effects on phytoplankton in Piscivore Lake were
likely to be caused by the high Daphnia biomass. It
is worth mentioning that extremely stable thermal
stratification in both Gräfenhain lakes almost prevents mixing of hypolimnetic water rich in phosphorus into the epilimnion during summer. This
together with low external P-loading (almost zero
during summer) allows total P concentration to
decrease in Piscivore Lake although the relatively
high total P concentration points to an eutrophic
lake. This re-emphasises that, at least in deep lakes,
BEThP must be defined in terms of P-loading rather
than concentration.
In conclusion, the effect of biomanipulation in deep
slightly eutrophic or mesotrophic lakes with P-loadings below BEThP is twofold (Fig. 6): edible phytoplankton is controlled top-down by strong grazing
and, perhaps more importantly, total phytoplankton is
bottom-up controlled by a biomanipulation-induced
reduction of phosphorus availability. As the efficacy of
the second (indirect) mechanism is limited to an
intermediate level of P-availability (see above), the
high incidence of successful biomanipulation in deep
lakes of slightly eutrophic or mesotrophic state, which
meet this criterion, becomes clear. Together with the
considerations about biomanipulation in oligotrophic
lakes (see below), these conclusions add a completely
new aspect to the ‘mesotrophic maximum hypothesis’
proposed by Elser & Goldman (1991) on the basis of
short-term enclosure experiments.
Long-term experiments in eutrophic
and hypertrophic deep lakes
In long-term (>3–5 years) whole-lake biomanipulation
studies in eutrophic and hypertrophic deep lakes with
P concentrations above BEThP, no sustained reduction of total phytoplankton biomass during midsummer has been observed (e.g. Benndorf et al., 1988;
Kasprzak, Krienitz & Koschel, 1993; Drenner et al.,
2000). Top-down control of phytoplankton in these
Fig. 6 Schematic diagram showing changes in biomass (or P
concentration) and sign of correlations between biomass (or P
concentration) of adjacent trophic levels under strong top-down
control in long-term experiments in deep mesotrophic or slightly
eutrophic lakes. Dashed arrow indicates enhanced epilimnetic
P-losses caused by a high biomass of large-sized herbivorous
zooplankton.
lakes was limited to temporal biomass reductions
during a short clear-water phase in spring and shifts
of the phytoplankton community towards inedible
forms. Comparative observations in unmanipulated
eutrophic and hypertrophic lakes revealed almost
identical results (e.g. Sommer et al., 1986; Kasprzak,
Lathrop & Carpenter, 1999).
The described pattern of phytoplankton response to
top-down impacts in eutrophic and hypertrophic
lakes is exemplified by the long-term experiment in
Bautzen Reservoir (see Benndorf, 1995; Benndorf &
Schultz, 2000, for details). Although a strong reduction of the edible fraction was evident, no sustained
reduction of the total phytoplankton biomass was
found after 1981, the first biomanipulation year
(Fig. 7). On the contrary, total phytoplankton biomass
increased during the biomanipulation period until
about 1992 ⁄ 1993. This increase reflects the simultaneous increase in external P-loading (Benndorf, 1995)
and in-lake total P concentration (Fig. 7). With
decreasing external P-loading and in-lake total P concentration between 1993 and 1999, a phytoplankton
biomass comparable to the pre-biomanipulation per 2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295
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2289
Fig. 7 Biovolume of edible and inedible
phytoplankton (summer averages, May to
October) and concentration of total phosphorus (annual averages) in Bautzen
Reservoir (Germany) before and during
biomanipulation (see Benndorf, 1995;
Benndorf & Schultz, 2000, for experimental details; external P-loading was
dramatically reduced after 1990) (extended from Benndorf, 1995).
iod was observed (Fig. 7). Thus, summer averages of
total phytoplankton biomass reflect the long-term
changes in phosphorus availability rather than the
influence of biomanipulation. As expected according
to the BEThP hypothesis, total P in this hypertrophic
reservoir was not reduced by biomanipulation, thus
indicating that P-loading was far above BEThP (Fig. 8,
top). Nevertheless, despite the increased phytoplankton biomass, water transparency remained almost
unchanged during about 80% of all sampling dates
and even improved in 20% of all cases (samples taken
during the clear-water phase) under biomanipulation
conditions (Fig. 8, bottom). This apparent contradiction between increased total P concentration and
phytoplankton biomass on the one hand, and similar
or even greater water transparency on the other
hand, was caused by structural changes in the phytoplankton community (i.e. lower light scattering of
large-sized algae compared with small-sized phytoplankton).
Findings from other whole-lake experiments in
deep eutrophic and hypertrophic lakes revealing
top-down control of total phytoplankton biomass
(e.g. Oskam, 1978; Vanni et al., 1990; Lathrop,
Carpenter & Robertson, 1999; Carpenter et al., 2001)
seem to be at variance with the findings above. How
can this discrepancy be reconciled? Low light availability resulting from either enhanced vertical mixing
(Oskam, 1978; Vanni et al., 1990; Lathrop et al., 1999)
or high light attenuation (water colour) (Carpenter
et al. 2001) apparently inhibited the development
of inedible phytoplankton in those experiments
suggesting that strong light limitation in lakes with
P-loadings well above BEThP can result in the same
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295
Fig. 8 Cumulative frequency distributions of total phosphorus
(P) and Secchi depth in Bautzen Reservoir (Germany) before and
during biomanipulation (original data). Only summer values
(May to October) are shown. Periods as in Fig. 7 (see Benndorf,
1995; Benndorf & Schultz, 2000, for experimental details).
final outcome as a reduction of P-loading below
BEThP (Oskam, 1978; Benndorf, 1995).
We conclude that in deep eutrophic and hypertrophic lakes, P-loading is too high (>BEThP) to allow
an indirect bottom-up control of phytoplankton by a
biomanipulation-induced reduction of the total
P-content in the epilimnion. With the exception of
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J. Benndorf et al.
Fig. 9 Schematic diagram showing changes in biomass (or P
concentration) and sign of correlation between biomass (or P
concentration) of adjacent trophic levels under strong top-down
control in long-term experiments in deep eutrophic and hypertrophic lakes. Lakes characterised by strong light limitation
(high mixing depth; high light attenuation coefficient) are
excluded.
lakes characterised by enhanced light limitation of
primary production, there is no correlation between
herbivorous zooplankton and the biomass of total
primary producers (edible and inedible phytoplankton). The biomass of total primary producers is
mainly controlled bottom-up as indicated by the
positive correlation coefficient (Fig. 9). Slightly
increased water transparency seems to be the only
(although not unimportant) benefit of biomanipulation in deep lakes having P-loadings above BEThP.
Strong light limitation as a result of high mixing
depth and ⁄ or light attenuation shifts the phytoplankton response to biomanipulation of eutrophic and
hypertrophic lakes towards the response pattern
described for mesotrophic and slightly eutrophic
lakes.
Long-term experiments in oligotrophic deep lakes
The role of an upper threshold of P-availability that
cannot be exceeded without negative consequences
for effective biomanipulation, is increasingly accep-
ted, whereas the existence of a lower P-threshold for
effective biomanipulation has been rarely recognised.
It has been argued that zooplankton biomass might
be too low to control phytoplankton under oligotrophic and ultraoligotrophic conditions (e.g. Elser &
Goldman, 1991). However, when P-availability and
hence primary production are low, herbivorous
zooplankton can still maintain a relatively high
biomass provided that predation losses are low (Bürgi
et al., 1999). Consequently, low predation losses of
zooplankton (i.e. biomanipulation conditions) should
cause effective control of edible phytoplankton also
under oligotrophic conditions (Lampert, 1988; Kamjunke et al., 1996). Low zooplankton biomass therefore
can hardly explain the existence of a lower biomanipulation efficiency threshold of P-availability.
However, at exceedingly low P concentrations (e.g.
6–7 lg L)1 total P), total phytoplankton biomass may
not be reduced under biomanipulation conditions
(Ramcharan et al., 1995; McQueen et al., 2001). This
finding is consistent with the BEThP hypothesis,
however, and need not be associated with a low
zooplankton biomass. If the sustained reduction of
total phytoplankton biomass is closely related to a
biomanipulation-induced decrease in total P (see
above), the total P concentration cannot be lowered
below a certain (low) threshold. This threshold would
result from the balance between processes causing
decreases (see above) and increases in total P (including P-remobilization by zooplankton and fish; see
Andersson et al., 1988).
Guy, Taylor & Carter (1994) have identified the
mean decline of total P during summer stagnation in
the upper 10 m of 10 oligotrophic and mesotrophic
lakes. The decline rate was significantly correlated
with the total P concentration at the onset of the
summer stagnation period (Fig. 10). The intersection
of the regression line with the x-axis represents the
lower threshold below which the total P concentration
cannot be brought by any means (including biomanipulation-enhanced P reduction). The threshold of
about 5 lg L)1 is very similar to the total P concentration in oligotrophic lakes (6–7 lg L)1) where biomanipulation failed to reduce the total P concentration
and (according to the BEThP hypothesis) phytoplankton biomass (Ramcharan et al., 1995). Figure 10 shows,
furthermore, that relatively strong declines in total P
concentration (near 0.05 lg L)1 day)1) were found
only in mesotrophic lakes having spring concentra 2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295
Top-down control of phytoplankton
2291
Fig. 10 Relationship between mean daily decline in total phosphorus (TP) during the summer stagnation period (150 days)
and spring concentration of total phosphorus in 10 oligo to
mesotrophic lakes in Ontario (Canada). Source data from Guy
et al. (1994).
tions > 10 lg L)1. This observation further supports
our conclusion above in the discussion of long-term
experiments in mesotrophic and slightly eutrophic
lakes.
Here we conclude that in oligotrophic deep lakes
total P concetrations are too low to exacerbate
P-limitation of phytoplankton further by a biomanipulation-induced P-reduction. Phytoplankton in these
lakes is mainly controlled bottom-up, as the positive
correlation coefficient between P and total phytoplankton indicates (Fig. 11).
General conclusions
Time scale, lake depth and nutrient status proved
to be the decisive factors determining the success
or failure of biomanipulation of pelagic food webs.
Successful top-down control of phytoplankton can be
expected in short-term experiments, in shallow lakes
and in mesotrophic and slightly eutrophic deep lakes.
Top-down control of total phytoplankton biomass
cannot be expected over longer periods (e.g. whole
summer) in neither highly eutrophic and hypertrophic nor oligotrophic deep lakes. However, in highly
eutrophic and hypertrophic deep lakes, short clearwater phases (analogous to successful phytoplankton
control in short-term experiments) and changes in the
phytoplankton composition can cause improved
water transparency.
The main objective of this review was to elucidate
the boundary conditions under which sustained
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295
Fig. 11 Schematic diagram showing changes in biomass (or P
concentration) and sign of correlations between biomass (or P
concentration) of adjacent trophic levels under strong top-down
control in long-term experiments in deep oligotrophic to
ultraoligotrophic lakes. Cross indicates that low TP concentrations (about 5 lg L)1) impede enhanced epilimnetic P-losses
because of high biomass of large-sized herbivorous
zooplankton.
reduction of phytoplankton biomass by biomanipulation can be achieved. The evaluation of the three
conditions considered leads to the following general
conclusions regarding biomanipulation as a tool
in water quality management: (1) long-term (whole
summer, many years) success is more constrained than
success in the short term (e.g. a 3-week clear-water
phase). (2) Long-term success is more likely to be
achieved in shallow lakes where macrophytes can
suppress phytoplankton development. (3) High external and internal P-loading of highly eutrophic and
hypertrophic deep lakes should be lowered to such an
extent that a biomanipulation efficiency threshold of
P-loading (BEThP) is no longer exceeded. If this is not
feasible, enhancement of light limitation (e.g. by
artificial destratification) provides an alternative management strategy. (4) In deep lakes experiencing low
P-loadings (i.e. loadings below BEThP; mesotrophic and
slightly eutrophic lakes), biomanipulation can induce a
considerable reduction in the in-lake P concentration
and thus cause real ‘oligotrophication’. (5) There is
almost no possibility (and from the viewpoint of lake
2292
J. Benndorf et al.
management also no need) to exert top-down control
on total phytoplankton biomass in oligotrophic lakes.
(6) With the exception of short-term effects observed in
enclosure studies or during short clear-water phases,
control of phytoplankton biomass under all other
boundary conditions is based on indirect top-down
effects, including bottom-up feedback mechanisms,
rather than on direct top-down control by grazing.
Consequently, both shallow and deep lakes lend
themselves to biomanipulation. The effectiveness of
biomanipulation depends on the P-availability in both
lake types. In deep lakes, biomanipulation efficiency
approaches a maximum within a range of P-availability defined by the BEThP of 0.6–0.8 g total P m)2 year)1 (upper limit) and a minimum in-lake total P
concentration of about 5–10 lg L)1 (lower limit).
Management strategies should hence start by reducing external and internal P-loadings of highly eutrophic and hypertrophic lakes below BEThP. The
resulting slightly eutrophic or mesotrophic state can
then be further improved by top-down control measures. Improvement of water quality beyond the slightly
eutrophic or mesotrophic state seems not to be costeffective by loading reduction alone. Therefore, the
need to combine biomanipulation with phosphorus
load reduction is increasingly accepted as a sustainable
and economically sound strategy in eutrophication
control (Lathrop et al., 1999; Meijer et al., 1999; Nicholls,
1999; Tallberg et al., 1999; Jeppesen et al., 2000).
Acknowledgments
We would like to thank G. Egerer and A. Benndorf
for technical support and G. Herrmann, V. Faltin,
S. Noack, S. Horn and K. Siemens for phytoplankton
analyses and data processing. Furthermore, we thank
Mark Gessner, Charles Ramcharan and two anonymous reviewers for valuable comments on the manuscript and Myriam Beaulne and Mark Gessner for
linguistic improvement of the text. Financial support
was provided by the Federal Ministry of Education
and Research (BMBF), Germany (grant nos. 0339423A
and 0339549).
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