Freshwater Biology (2002) 47, 2282–2295

Top-down control of : the role of time scale, lake depth and trophic state

JU¨ RGEN BENNDORF, WIEBKE BO¨ ING,* JOCHEN KOOP and IVONNE NEUBAUER 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.

SUMMARY 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 character- ised 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, phyto- plankton, water management, whole-lake experiments

trophic level (phytoplankton). The competing bottom- Introduction up ⁄top-down hypothesis (McQueen, Post & Mills, Both the biomanipulation concept (Shapiro, Lamarra 1986) predicts that top-down effects are strong at the & Lynch, 1975) and the trophic cascade hypothesis top of the food web and weaken towards the bottom, (Carpenter, Kitchell & Hodgson, 1985) are based on because phytoplankton biomass is thought to be more the fundamental assumption that a change in predator strongly controlled by resources (bottom-up) than by biomass at the highest trophic level of an aquatic food grazing (top-down). In an evaluation of 33 whole-lake web (piscivorous fish) cascades down to the lowest biomanipulation experiments, Reynolds (1994) con- cluded that top-down effects at the lower trophic Correspondence: Ju¨rgen Benndorf, Institute of Hydrobiology, levels are not the rule: 11 experiments support the Dresden University of Technology, Mommsenstr. 13, D-01062 biomanipulation ⁄trophic cascade hypothesis whereas Dresden, Germany. E-mail: [email protected] 16 experiments support the bottom-up ⁄top-down

2282 2002 Blackwell Science Ltd Top-down control of phytoplankton 2283 hypothesis. The remaining six experiments provided experiments in mesotrophic (or slightly eutrophic) inconclusive answers. As both hypotheses were thus deep lakes, (iv) long-term experiments in eutrophic refuted by a number of cases, neither can be regarded and hypertrophic deep lakes and (v) long-term to be generally valid. The validity of both is obviously experiments in oligotrophic deep lakes. These five restricted to certain boundary conditions. categories encompass all the important combinations In this review, we explore the boundary conditions of the three above-mentioned boundary conditions. required for top-down control of phytoplankton We suppose in all cases discussed in this review a biomass. These boundary conditions are seemingly successful enhancement of large-sized herbivorous the same as that of the assumptions underlying the by an appropriate management of the trophic cascade hypothesis. However, it must be fish community. Case studies (or periods) not fulfil- emphasised that there are two quite different theor- ling this prerequisite were excluded. etical possibilities to achieve top-down control of phytoplankton, namely (1) by a strong direct casca- Short-term experiments in enclosures ding effect on phytoplankton biomass (grazing by zooplankton), or (2) by strong direct cascading effects Strong top-down effects on phytoplankton biomass of zooplankton on phytoplankton resources rather were demonstrated in numerous enclosure experi- than on biomass. In the second case, phytoplankton ments (e.g. Elser & Goldman, 1991; Kurmayer & biomass is reduced by an indirect cascading effect Wanzenbo¨ck, 1996; Vanni & Layne, 1997; Bertolo passing through a positive feedback (bottom-up) et al., 2000). However, because of the large difference between resources and phytoplankton. Possibility (1) in scales, it is questionable whether these findings can is consistent with the trophic cascade hypothesis (i.e. be transferred to whole lakes (Carpenter, 1996). In all trophic levels down to phytoplankton and dis- addition to large differences in spatial scales, enclo- solved phosphate are negatively correlated), whereas sure experiments are also unrealistically short. They possibility (2) emerges from the bottom-up ⁄top-down usually must be terminated after 4–6 weeks because hypothesis (i.e. higher trophic levels are negatively of excessive algal growth on the enclosure walls, even correlated; lower trophic levels reveal positive corre- in mesotrophic and oligotrophic lakes. Four to six lation coefficients). However, as biomanipulation weeks are too short for phytoplankton to reach a new success is mainly judged by water transparency and ‘steady-state’ fully adapted to strong top-down phytoplankton biomass (Drenner & Hambright, 1999), effects. This is demonstrated by results from hyper- both possibilities – regardless of their attribution to the trophic Bautzen Reservoir (Germany) in combination respective hypothesis – would considerably enhance with a concurrent enclosure experiment in a nearby the chance for successful application of biomanipula- small lake (Bo¨ing et al., 1998). tion as a tool in water quality management. Total chlorophyll a concentrations in enclosures The main focus of this review consists in identi- containing large Daphnia (Daphnia pulex Leydig, fying the respective boundary conditions responsible D. rosea Leydig) were severely reduced by day 36 for the implementation of the two possibilities to irrespective of the nutrient content (Fig. 1, left). On the reduce phytoplankton by biomanipulation. Based on other hand, the proportion of inedible phytoplankton comprehensive comparative studies (e.g. Reynolds, increased from less than 10% at the beginning to 1994; McQueen, 1998; Drenner & Hambright, 1999; about 50% on day 36 (Fig. 1, middle-left). We do not Meijer et al., 1999; Jeppesen et al., 2000) and our own know whether this development towards more ined- experience (e.g. Benndorf, 1987, 1990, 1995; Benndorf ible phytoplankton would have continued had the et al., 2000; Wissel et al., 2000), we assume that three experiment not been terminated. If so, the low total conditions may be particularly important in this chlorophyll a concentration at the end of the experi- context: time scale, lake depth and trophic state. The ment must be regarded as transient after a distur- role of these conditions in top-down control of bance. Evidence for this view emerges from the phytoplankton will be evaluated using case studies phytoplankton development during the same period carried out in five types of freshwater systems: in the whole-lake biomanipulation experiment in (i) short-term experiments in enclosures, (ii) long- Bautzen Reservoir (see Benndorf & Schultz, 2000, for term experiments in shallow lakes, (iii) long-term experimental conditions). As soon as the filtration rate

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 2284 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 Bo¨ing et al., 1998) under strong Daphnia-grazing pressure. Experimental conditions of the ) ) enclosure experiment (arithmetic mean ± 1 SD): C: control (TP ¼ 84 ± 25 lgL 1;TN¼ 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 lgL 1;TN¼ 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 lgL 1;TN¼ 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 lgL 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 lgL 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 mid- with enclosure results is noteworthy. Only after this May (day 0 in Fig. 1, right), both edible and inedible ‘transient phase’ did inedible phytoplankton (mainly phytoplankton was suppressed for about 5 weeks Microcystis spp.) start exponential growth and reach (until day 36 in Fig. 1, right). The complete agreement high biomass at the end of the clear-water phase (day

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 Top-down control of phytoplankton 2285 78 in Fig. 1, right). Although the filtration rate of <3 m (Gulati et al., 1990; Reynolds, 1994; Drenner & daphnids fluctuated considerably during that period, Hambright, 1999; Meijer et al., 1999). The main reason ) ) it never dropped below 0.1 L L 1 day 1 and peaked as is that shallow lakes may occur in two alternative ) ) high as 1.1 L L 1 day 1 (see Bo¨ing et al., 1998). Thus, stable states, a turbid phytoplankton-dominated state the grazing pressure in enclosures and in the whole- and a clear-water state characterised by dense stands lake experiment was high and comparable during the of submerged macrophytes (Moss, 1990; Blindow observation period shown in Fig. 1. et al., 1993; Perrow et al., 1997; Scheffer, 1998). The This comparison of phytoplankton development in clear-water state is more likely at low phosphorus two systems under strong grazing pressure confirms levels and high grazing pressure on phytoplankton previous conclusions (Reynolds, 1994; Carpenter, (Jeppesen et al., 1997, 2000; Meijer et al., 1999). 1996) that the short time scale of enclosure experi- Enhanced grazing pressure by biomanipulation is ments prevents the development of slow-growing only critical, however, as long as dense macrophyte large (inedible) phytoplankton which in the long-term stands are lacking (Persson et al., 1993; Perrow et al., will fill in the niches opened by intense grazing (cf. 1997; Meijer et al., 1999). Numerous studies have Gliwicz, 1975, 1990, 2002). Enclosure experiments, indeed shown a negligible top-down control of phy- therefore, tend to support the cascade theory (Fig. 2), toplankton under clear-water conditions (macrophyte but their findings are largely irrelevant for whole-lake dominance) during summer (e.g. Meijer et al., 1999; situations (e.g. Kasprzak & Lathrop, 1997). This Blindow et al., 2000; Declerck et al., 2000). Therefore, conclusion, of course, does not preclude the useful- mechanisms other than grazing pressure must affect ness of enclosure experiments for studying short-term phytoplankton biomass under conditions of macro- processes (e.g. Lyche et al., 1996; Vanni & Layne, phyte dominance. 1997). Indirect bottom-up effects are likely also to play an important role in suppressing phytoplankton once macrophytes are established. Greater nitrogen Long-term experiments in shallow lakes limitation as a result of enhanced nitrification ⁄deni- There is overwhelming evidence that biomanipulation trification in the sediment (Jeppesen et al., 1998) and is most successful in shallow lakes with a mean depth competition for nitrogen between phytoplankton and macrophytes (Declerck et al., 2000) are such indirect effects. The release of allelopathic com- pounds by macrophytes might be just as important (Declerck et al., 2000). Groß, Meyer & Schilling (1996), for example, detected in Myriophyllum spica- tum L. an algicidal polyphenol (tellimagrandin II), which inhibited algal extracellular enzymes, includ- ing alkaline phosphatase. Inhibition of alkaline phosphatase by macrophytes has also been observed by Yiyong, Jianqiu & Yongqing (2000). This mechan- ism may explain why clear-water states are more stable at low phosphorus concentrations: the com- petitive advantage of macrophytes resulting from the inhibition of algal phosphatase is reduced (or eliminated) when ortho-phosphate concentrations 3 (PO4 –P) are high. Inedible phytoplankton usually develops sooner or later under strong top-down control in deep lakes without macrophytes (see above). Similar mass devel- Fig. 2 Schematic diagram showing changes in biomass (or P opments are uncommon in macrophyte-dominated concentration) and sign of correlations between biomass (or P concentration) of adjacent trophic levels under strong top-down shallow lakes, even when grazing pressure is strong control in short-term experiments (e.g. enclosure studies). (Gulati, 1995). Allelopathy and nitrogen limitation

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 2286 J. Benndorf et al. might account for this phenomenon. However, sus- Long-term experiments in mesotrophic tained clear-water states during summer have also and slightly eutrophic deep lakes been reported from shallow sewage ponds lacking macrophytes (Uhlmann, 1955). Consequently, other Striking differences in phytoplankton reduction by mechanisms preventing the mass development of biomanipulation in deep lakes (mean depth >5 m) are inedible phytoplankton under strong Daphnia grazing caused by differences in phosphorus (P) loading. in shallow waterbodies can also occur. Whereas eutrophic and hypertrophic lakes usually Thus, earlier conclusions (Gulati et al., 1990; show only a temporal reduction in phytoplankton Reynolds, 1994; Drenner & Hambright, 1999; Meijer biomass (clear-water phase in spring or early summer, et al., 1999) can be confirmed that a trophic cascade e.g. Lampert et al., 1986; Sommer et al., 1986), strong down to the phytoplankton level is found in long- top-down control in deep mesotrophic to slightly term biomanipulation experiments in shallow lakes eutrophic lakes can cause sustained phytoplankton (Fig. 3). However, mechanisms other than top-down biomass reductions (Stenson et al., 1978; Stenson, effects are also involved. Bottom-up effects dominate 1988; Wissel et al., 2000). The key factor for this the trophic interactions between lower trophic levels difference might consist in the biomanipulation- as demonstrated by positive correlations between induced reduction of P-availability for phytoplankton zooplankton and macrophytes abundance and (Benndorf, 1992; Sterner, Elser & Hessen, 1992). The between total primary producers and phosphate most important mechanisms behind the reduced concentrations (Fig. 3). These bottom-up effects, how- P-availability are (1) enhanced vertical P-translocation ever, are at least partly induced by top-down control. through sedimentation, or migration (Wright & The key factor for this is shallow depth allowing Shapiro, 1984; Andersson, Graneli & Stenson, 1988; macrophytes to become dominant (inedible) primary Bloesch & Bu¨ rgi, 1989; Mazumder et al., 1992) and (2) producers. 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 Bioma- nipulation Efficiency Threshold of P-loading; Benn- dorf, 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 compen- sated 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 concentra- Fig. 3 Schematic diagram showing changes in biomass (or P tion in shallow lakes as proposed by Jeppesen et al. concentration) and sign of correlations between biomass (or P concentration) of adjacent trophic levels under strong top-down (1990, 1997). The main requirement underlying the control in long-term experiments in shallow lakes. BEThP concept is to achieve a negative mass balance of

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 Top-down control of phytoplankton 2287

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.

Fig. 5 Cumulative frequency distributions of epilimnetic chlo- total P in the epilimnion (i.e. P-losses by sedimenta- rophyll a, epilimnetic total P concentration and P-sedimentation tion into the hypolimnion and flushing > external (measured in sediment traps according to Horn & Horn, 1990) in P-loading and import from the hypolimnion; Fig. 4). Planktivore Lake and Piscivore Lake in Gra¨fenhain, Germany This requirement can even be met at relatively high P (original data). Only summer values (June to August) during the period of optimum biomanipulation in Piscivore Lake and concentrations (see Fig. 5), but not when P-loading is extremely high planktivory in Planktivore Lake are shown (1996, high. Thus, it is impossible to convert the BEThP- 1998, 1999; see Wissel et al., 2000, for experimental design). ) ) estimate 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 vore Lake) was biomanipulated for many years with small deep quarry lakes in Gra¨fenhain near Dresden, moderate success (Benndorf et al., 1984, 2000). Bioma- Germany (Benndorf et al., 1984, 2000; Wissel et al., nipulation was finally most efficient after an ‘opti- 2000), provides an example in support of the BEThP mum’ fish density had been adjusted in 1996 (Wissel hypothesis. The external P-loading of both lakes is et al., 2000). The other lake (Planktivore Lake) was ) ) rather low (about 0.6 g P m 2 year 1, almost exclu- permanently colonised (except in 1997) by a dense sively because of fallen leaves), and internal P-loading population of a small planktivorous cyprinid, Leuc- has been greatly reduced by repeated sediment aspius delineatus L. (see Benndorf et al., 2000 and treatment with nitrate according to Ripl (1976). Total Wissel et al., 2000, for details). P-loading therefore is very probably below BEThP in Total chlorophyll a (including the inedible frac- both lakes. Additionally, the spring P concentration tion) during summer was distinctly lower in Pisci- has been reduced by artificially enhancing P-precipi- vore Lake compared with Planktivore Lake (Fig. 5, tation with Fe2(SO4)3 (see Wissel et al., 2000). After top). In contrast to highly eutrophic or hypertrophic nitrate treatment and P-precipitation, the lakes were lakes (see below), inedible phytoplankton was not in a slightly eutrophic state. One of the lakes (Pisci- able to completely fill the niche opened by intensive

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 2288 J. Benndorf et al. Daphnia grazing, not even during the entire sum- mer 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-sedimenta- tion (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 Gra¨fenhain lakes almost pre- vents mixing of hypolimnetic water rich in phos- phorus 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 Fig. 6 Schematic diagram showing changes in biomass (or P than concentration. concentration) and sign of correlations between biomass (or P In conclusion, the effect of biomanipulation in deep concentration) of adjacent trophic levels under strong top-down control in long-term experiments in deep mesotrophic or slightly slightly eutrophic or mesotrophic lakes with P-load- eutrophic lakes. Dashed arrow indicates enhanced epilimnetic ings below BEThP is twofold (Fig. 6): edible phyto- P-losses caused by a high biomass of large-sized herbivorous plankton is controlled top-down by strong grazing zooplankton. and, perhaps more importantly, total phytoplankton is bottom-up controlled by a biomanipulation-induced lakes was limited to temporal biomass reductions reduction of phosphorus availability. As the efficacy of during a short clear-water phase in spring and shifts the second (indirect) mechanism is limited to an of the phytoplankton community towards inedible intermediate level of P-availability (see above), the forms. Comparative observations in unmanipulated high incidence of successful biomanipulation in deep eutrophic and hypertrophic lakes revealed almost lakes of slightly eutrophic or mesotrophic state, which identical results (e.g. Sommer et al., 1986; Kasprzak, meet this criterion, becomes clear. Together with the Lathrop & Carpenter, 1999). considerations about biomanipulation in oligotrophic The described pattern of phytoplankton response to lakes (see below), these conclusions add a completely top-down impacts in eutrophic and hypertrophic new aspect to the ‘mesotrophic maximum hypothesis’ lakes is exemplified by the long-term experiment in proposed by Elser & Goldman (1991) on the basis of Bautzen Reservoir (see Benndorf, 1995; Benndorf & short-term enclosure experiments. Schultz, 2000, for details). Although a strong reduc- tion of the edible fraction was evident, no sustained reduction of the total phytoplankton biomass was Long-term experiments in eutrophic found after 1981, the first biomanipulation year and hypertrophic deep lakes (Fig. 7). On the contrary, total phytoplankton biomass In long-term (>3–5 years) whole-lake biomanipulation increased during the biomanipulation period until studies in eutrophic and hypertrophic deep lakes with about 1992 ⁄1993. This increase reflects the simulta- P concentrations above BEThP, no sustained reduc- neous increase in external P-loading (Benndorf, 1995) tion of total phytoplankton biomass during midsum- and in-lake total P concentration (Fig. 7). With mer has been observed (e.g. Benndorf et al., 1988; decreasing external P-loading and in-lake total P con- Kasprzak, Krienitz & Koschel, 1993; Drenner et al., centration between 1993 and 1999, a phytoplankton 2000). Top-down control of phytoplankton in these biomass comparable to the pre-biomanipulation per-

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 Top-down control of phytoplankton 2289

Fig. 7 Biovolume of edible and inedible phytoplankton (summer averages, May to October) and concentration of total phos- phorus (annual averages) in Bautzen Reservoir (Germany) before and during biomanipulation (see Benndorf, 1995; Benndorf & Schultz, 2000, for experi- mental details; external P-loading was dramatically reduced after 1990) (exten- ded 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 phytoplank- ton 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 contradic- tion 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 phyto- plankton community (i.e. lower light scattering of large-sized algae compared with small-sized phyto- plankton). Findings from other whole-lake experiments in deep eutrophic and hypertrophic lakes revealing Fig. 8 Cumulative frequency distributions of total phosphorus top-down control of total phytoplankton biomass (P) and Secchi depth in Bautzen Reservoir (Germany) before and (e.g. Oskam, 1978; Vanni et al., 1990; Lathrop, during biomanipulation (original data). Only summer values Carpenter & Robertson, 1999; Carpenter et al., 2001) (May to October) are shown. Periods as in Fig. 7 (see Benndorf, 1995; Benndorf & Schultz, 2000, for experimental details). seem to be at variance with the findings above. How can this discrepancy be reconciled? Low light avail- ability resulting from either enhanced vertical mixing final outcome as a reduction of P-loading below (Oskam, 1978; Vanni et al., 1990; Lathrop et al., 1999) BEThP (Oskam, 1978; Benndorf, 1995). or high light attenuation (water colour) (Carpenter We conclude that in deep eutrophic and hyper- et al. 2001) apparently inhibited the development trophic lakes, P-loading is too high (>BEThP) to allow of inedible phytoplankton in those experiments an indirect bottom-up control of phytoplankton by a suggesting that strong light limitation in lakes with biomanipulation-induced reduction of the total P-loadings well above BEThP can result in the same P-content in the epilimnion. With the exception of

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 2290 J. Benndorf et al. 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 oligo- trophic 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 (Bu¨ rgi 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; Kam- junke et al., 1996). Low zooplankton biomass therefore can hardly explain the existence of a lower biomanip- ulation efficiency threshold of P-availability. However, at exceedingly low P concentrations (e.g. ) 6–7 lgL 1 total P), total phytoplankton biomass may not be reduced under biomanipulation conditions (Ramcharan et al., 1995; McQueen et al., 2001). This Fig. 9 Schematic diagram showing changes in biomass (or P concentration) and sign of correlation between biomass (or P finding is consistent with the BEThP hypothesis, concentration) of adjacent trophic levels under strong top-down however, and need not be associated with a low control in long-term experiments in deep eutrophic and hyper- zooplankton biomass. If the sustained reduction of trophic lakes. Lakes characterised by strong light limitation total phytoplankton biomass is closely related to a (high mixing depth; high light attenuation coefficient) are excluded. biomanipulation-induced decrease in total P (see above), the total P concentration cannot be lowered below a certain (low) threshold. This threshold would lakes characterised by enhanced light limitation of result from the balance between processes causing primary production, there is no correlation between decreases (see above) and increases in total P (inclu- herbivorous zooplankton and the biomass of total ding P-remobilization by zooplankton and fish; see primary producers (edible and inedible phytoplank- Andersson et al., 1988). ton). The biomass of total primary producers is Guy, Taylor & Carter (1994) have identified the mainly controlled bottom-up as indicated by the mean decline of total P during summer stagnation in positive correlation coefficient (Fig. 9). Slightly the upper 10 m of 10 oligotrophic and mesotrophic increased water transparency seems to be the only lakes. The decline rate was significantly correlated (although not unimportant) benefit of biomanipula- with the total P concentration at the onset of the tion in deep lakes having P-loadings above BEThP. summer stagnation period (Fig. 10). The intersection Strong light limitation as a result of high mixing of the regression line with the x-axis represents the depth and ⁄or light attenuation shifts the phytoplank- lower threshold below which the total P concentration ton response to biomanipulation of eutrophic and cannot be brought by any means (including bioma- hypertrophic lakes towards the response pattern nipulation-enhanced P reduction). The threshold of ) described for mesotrophic and slightly eutrophic about 5 lgL 1 is very similar to the total P concentra- ) lakes. tion in oligotrophic lakes (6–7 lgL 1) where bioma- nipulation failed to reduce the total P concentration and (according to the BEThP hypothesis) phytoplank- Long-term experiments in oligotrophic deep lakes ton biomass (Ramcharan et al., 1995). Figure 10 shows, The role of an upper threshold of P-availability that furthermore, that relatively strong declines in total P ) ) cannot be exceeded without negative consequences concentration (near 0.05 lgL 1 day 1) were found for effective biomanipulation, is increasingly accep- 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 phos- phorus (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 lgL 1. This observation further supports our conclusion above in the discussion of long-term Fig. 11 Schematic diagram showing changes in biomass (or P experiments in mesotrophic and slightly eutrophic concentration) and sign of correlations between biomass (or P lakes. concentration) of adjacent trophic levels under strong top-down control in long-term experiments in deep oligotrophic to Here we conclude that in oligotrophic deep lakes ultraoligotrophic lakes. Cross indicates that low TP concentra- ) total P concetrations are too low to exacerbate tions (about 5 lgL 1) impede enhanced epilimnetic P-losses P-limitation of phytoplankton further by a biomanip- because of high biomass of large-sized herbivorous ulation-induced P-reduction. Phytoplankton in these zooplankton. lakes is mainly controlled bottom-up, as the positive correlation coefficient between P and total phyto- reduction of phytoplankton biomass by biomanipula- plankton indicates (Fig. 11). tion can be achieved. The evaluation of the three conditions considered leads to the following general conclusions regarding biomanipulation as a tool General conclusions in water quality management: (1) long-term (whole Time scale, lake depth and nutrient status proved summer, many years) success is more constrained than to be the decisive factors determining the success success in the short term (e.g. a 3-week clear-water or failure of biomanipulation of pelagic food webs. phase). (2) Long-term success is more likely to be Successful top-down control of phytoplankton can be achieved in shallow lakes where macrophytes can expected in short-term experiments, in shallow lakes suppress phytoplankton development. (3) High exter- and in mesotrophic and slightly eutrophic deep lakes. nal and internal P-loading of highly eutrophic and Top-down control of total phytoplankton biomass hypertrophic deep lakes should be lowered to such an cannot be expected over longer periods (e.g. whole extent that a biomanipulation efficiency threshold of summer) in neither highly eutrophic and hypertro- P-loading (BEThP) is no longer exceeded. If this is not phic nor oligotrophic deep lakes. However, in highly feasible, enhancement of light limitation (e.g. by eutrophic and hypertrophic deep lakes, short clear- artificial destratification) provides an alternative man- water phases (analogous to successful phytoplankton agement strategy. (4) In deep lakes experiencing low control in short-term experiments) and changes in the P-loadings (i.e. loadings below BEThP; mesotrophic and phytoplankton composition can cause improved slightly eutrophic lakes), biomanipulation can induce a water transparency. considerable reduction in the in-lake P concentration The main objective of this review was to elucidate and thus cause real ‘oligotrophication’. (5) There is the boundary conditions under which sustained almost no possibility (and from the viewpoint of lake

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 2292 J. Benndorf et al. management also no need) to exert top-down control Benndorf J. (1987) Food web manipulation without on total phytoplankton biomass in oligotrophic lakes. nutrient control: a useful strategy in lake restoration? (6) With the exception of short-term effects observed in Schweizerische Zeitschrift fu¨r Hydrologie, 49, 237–248. enclosure studies or during short clear-water phases, Benndorf J. (1990) Conditions for effective biomanipula- control of phytoplankton biomass under all other tion; conclusions derived from whole-lake experiments in Europe. Hydrobiologia, 200/201, 187–203. boundary conditions is based on indirect top-down Benndorf J. (1992) The control of indirect effects of effects, including bottom-up feedback mechanisms, biomanipulation. In: : Research and Appli- rather than on direct top-down control by grazing. cation to Water Supply (Eds D.W. Sutcliffe & J.G. Jones), Consequently, both shallow and deep lakes lend pp. 82–93. Freshwater Biological Association, Amble- themselves to biomanipulation. The effectiveness of side. biomanipulation depends on the P-availability in both Benndorf J. (1995) Possibilities and limits for controlling lake types. In deep lakes, biomanipulation efficiency eutrophication by biomanipulation. Internationale Revue approaches a maximum within a range of P-availab- der Gesamten Hydrobiologie, 80, 519–534. ) ility defined by the BEThP of 0.6–0.8 g total P m 2 - Benndorf J., Kneschke H., Kossatz K. & Penz E. (1984) ) year 1 (upper limit) and a minimum in-lake total P Manipulation of the pelagic food web by stocking with ) concentration of about 5–10 lgL 1 (lower limit). predacious fishes. Internationale Revue der Gesamten Management strategies should hence start by redu- Hydrobiologie, 69, 407–428. Benndorf J. & Miersch U. (1991) Phosphorus loading cing external and internal P-loadings of highly eutro- and efficiency of biomanipulation. Verhandlungen der phic and hypertrophic lakes below BEThP. The Internationalen Vereinigung fu¨r Theoretische und Ange- resulting slightly eutrophic or mesotrophic state can wandte Limnologie, 24, 2482–2488. then be further improved by top-down control meas- Benndorf J. & Schultz H. (2000) Talsperre Bautzen – ures. Improvement of water quality beyond the slightly Langzeit-Biomanipulation bei sehr hoher Na¨hrstoffbe- eutrophic or mesotrophic state seems not to be cost- lastung. In: Fischerei und Fischereiliches Management an effective by loading reduction alone. Therefore, the Trinkwassertalsperren (Eds H. Willmitzer, M.-G. Werner need to combine biomanipulation with phosphorus & W. Scharf), pp. 73–79. ATT-Technische Informatio- load reduction is increasingly accepted as a sustainable nen no. 11, Kommissionsverlag R. Oldenbourg, Mu¨ n- and economically sound strategy in eutrophication chen. control (Lathrop et al., 1999; Meijer et al., 1999; Nicholls, Benndorf J., Schultz H., Benndorf A. et al. (1988) Food- 1999; Tallberg et al., 1999; Jeppesen et al., 2000). web manipulation by enhancement of piscivorous fish stocks: Long-term effects in the hypertrophic Bautzen reservoir. Limnologica, 19, 97–110. Acknowledgments Benndorf J., Wissel B., Sell A.F., Hornig U., Ritter P. & Bo¨ing W. (2000) Food web manipulation by extreme We would like to thank G. Egerer and A. Benndorf enhancement of piscivory: an invertebrate predator for technical support and G. Herrmann, V. Faltin, compensates for the effects of planktivorous fish on a S. Noack, S. Horn and K. Siemens for phytoplankton plankton community. Limnologica, 30, 235–245. analyses and data processing. Furthermore, we thank Bertolo A., Lacroix G., Lescher-Moutoue F. & Cardinal- Mark Gessner, Charles Ramcharan and two anony- Legrand C. (2000) Plankton dynamics in planktivore- mous reviewers for valuable comments on the manu- and piscivore-dominated mesocosms. Archiv fu¨r script and Myriam Beaulne and Mark Gessner for Hydrobiologie, 147, 327–349. linguistic improvement of the text. Financial support Blindow I., Andersson G., Hargeby A. & Johansson S. was provided by the Federal Ministry of Education (1993) Long-term pattern of alternative stable states in two shallow eutrophic lakes. Freshwater Biology, 30, and Research (BMBF), Germany (grant nos. 0339423A 159–167. and 0339549). Blindow I., Hargeby A., Wagner B.M.A. & Andersson G. (2000) How important is the crustacean plankton for References the maintenance of water clarity in shallow lakes with abundant submerged vegetation? Freshwater Biology, Andersson G., Graneli W. & Stenson J. (1988) The 44, 185–197. influence of animals on phosphorus cycling in lake Bloesch J. & Bu¨ rgi H.R. (1989) Changes in phytoplankton . Hydrobiologia, 170, 267–284. and zooplankton biomass and composition reflected

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 Top-down control of phytoplankton 2293

by sedimentation. Limnology and Oceanography, 34, Gulati R.D. (1995) Food-chain manipulation as a tool in 1048–1061. management of small lakes in the Netherlands: the Bo¨ing W., Wagner A., Voigt H., Deppe T. & Benndorf J. Lake Zwemlust example. In: Biomanipulation in Lakes (1998) Phytoplankton responses to grazing by Daphnia and Reservoirs Management (Eds R. De Bernardi & G. galeata the biomanipulated Bautzen reservoir. Giussani), pp. 147–161. Guidelines of Lake Manage- Hydrobiologia, 389, 101–114. ment 7, Otsu, Japan. Bu¨ rgi H.R., Heller C., Gaebel S., Mookerji N. & Ward J.V. Gulati R.D., Lammens E.H.R.R., Meijer M.-L. & van Donk (1999) Strength of coupling between phyto- and E. (Eds) (1990) Biomanipulation – Tool for Water Man- zooplankton in Lake Lucerne (Switzerland) during agement. Kluwer Academic Publishers, Dordrecht. phosphorus abatement subsequent to a weak eutro- Guy M., Taylor W.D. & Carter J.C.H. (1994) Decline in phication. Journal of Plankton Research, 21, 485–507. total phosphorus in the surface waters of lakes Carpenter S.R. (1996) Microcosm experiments have during summer stratification, and its relationship limited relevance for community and ecol- to size distribution of particles and sedimentation. ogy. Ecology, 77, 677–680. Canadian Journal of Fisheries and Aquatic Sciences, 51, Carpenter S.R., Kitchell J.F. & Hodgson J.R. (1985) 1330–1337. Cascading trophic interactions and lake productivity. Horn W. & Horn H. (1990) A simple and reliable method Bioscience, 35, 634–639. for the installation of sediment traps in lakes. Carpenter S.R., Cole J.J., Hodgson J.R., Kitchell J.F., Pace Internationale Revue der Gesamten Hydrobiologie, 75, 269– M.L., Bade D., Cottingham K.L., Essington T.E., 270. Houser J.N. & Schindler D.E. (2001) Trophic cascades, Jeppesen E., Jensen J.P., Kristensen P., Søndergaard M., nutrients, and lake productivity: whole-lake experi- Mortensen E., Sortkjær O. & Olrik K. (1990) Fish ments. Ecological Monographs, 71, 163–186. manipulation as a restoration tool in shallow, eu- Declerck S., De Mester L., De Smedt P., Rommens W., trophic temperate lakes 2: threshold levels, long-term Vyverman W., Geenens V., Van Wichelen J., Degans H. stability and conclusions. Hydrobiologia, 200 ⁄201, 219– & Decleer K. (2000) Clear water and charophytes in a 227. hypertrophic pond. Verhandlungen der Internationalen Jeppesen E., Jensen J.P., Søndergaard M., Lauridsen T., Vereinigung fu¨r Theoretische und Angewandte Limnologie, Pedersen L.J. & Jensen L. (1997) Top-down control in 27, 541. freshwater lakes: the role of nutrient state, submerged Drenner R.W. & Hambright K.D. (1999) Biomanipulation macrophytes and water depth. Hydrobiologia, 342/343, of fish assemblages as a lake restoration technique. 151–164. Archiv fu¨r Hydrobiologie, 146, 129–165. Jeppesen E., Jensen J.P., Søndergaard M., Lauridsen T., Drenner R., Baca R., Ernst M., Jensen D. & Marshall D. Møller P.H. & Sandby K. (1998) Changes in nitrogen (2000) Experimental biomanipulation of a water sup- retention in shallow eutrophic lakes following a ply reservoir by stocking piscivorous largemouth bass. decline in density of cyprinids. Archiv fu¨r Hydrobiologie, Verhandlungen der Internationalen Vereinigung fu¨r Theo- 142, 129–151. retische und Angewandte Limnologie, 27, 542. Jeppesen E., Jensen J.P., Søndergaard M., Lauridsen T. & Elser J.J. & Goldman C.R. (1991) Zooplankton effects on Landkildehus F. (2000) Trophic structure, species phytoplankton in lakes of contrasting trophic status. richness and biodiversity in Danish lakes: changes Limnology and Oceanography, 36, 64–90. along a phosphorus gradient. Freshwater Biology, 45, Gliwicz Z.M. (1975) Effect of zooplankton grazing on 201–218. photosynthetic activity and composition of phyto- Kamjunke N., Herbst R.F., Wagner A. & Benndorf J. plankton. Verhandlungen der Internationalen Vereinigung (1996) Size distribution of primary production in a fu¨r Theoretische und Angewandte Limnologie, 19, 1490– whole-lake biomanipulation experiment under hyper- 1497. trophic conditions. Archiv fu¨r Hydrobiologie, 138, 259– Gliwicz Z.M. (1990) Why do cladocerans fail to control 271. algal blooms? Hydrobiologia, 200 ⁄201, 83–97. Kasprzak P., Krienitz L. & Koschel R. (1993) Biomanipu- Gliwicz Z.M. (2002) On the different nature of top-down lation: a limnological in-lake ecotechnology of eutro- and bottom-up effects in pelagic food webs. Freshwater phication management? Memorie Dell’istituto Italiano de Biology, 47, 2296–2312. Idrobiologia, 52, 151–169. Groß E.M., Meyer H. & Schilling G. (1996) Release and Kasprzak P. & Lathrop R.C. (1997) Influence of two ecological impact of algicidal hydrolysable polyphe- Daphnia species on summer phytoplankton assem- nols in Myriophyllum spicatum. Phytochemistry, 41, 133– blages from eutrophic lakes. Journal of Plankton 138. Research, 19, 1025–1044.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 2294 J. Benndorf et al.

Kasprzak P., Lathrop R.C. & Carpenter S.R. (1999) to the zebra mussel invasion. Journal of Great Lakes Influence of different sized Daphnia species on chlor- Research, 25, 942–949. ophyll concentration and summer phytoplankton Oskam G. (1978) Light and zooplankton as algae regu- community structure in eutrophic Wisconsin lakes. lating factors in eutrophic Biesbosch reservoirs. Journal of Plankton Research, 21, 2161–2174. Verhandlungen der Internationalen Vereinigung fu¨r Theo- Kurmayer R. & Wanzenbo¨ck J. (1996) Top-down effects retische und Angewandte Limnologie, 20, 1612–1618. of underyearling fish on a phytoplankton community. Perrow M.R., Meijer M.-L., Dawidowicz P. & Coop H. Freshwater Biology, 36, 599–609. (1997) Biomanipulation in shallow lakes: state of the Lampert W. (1988) The relationship between zooplankton art. Hydrobiologia, 342/343, 355–365. biomass and grazing: a review. Limnologica, 19, 11–20. Persson L., Johansson L., Andersson G., Diehl S. & Lampert W., Fleckner H., Rai H. & Taylor B.E. (1986) Hamrin S.F. (1993) Density dependent interactions in Phytoplankton control by grazing zooplankton: a lake ecosystems: whole lake perturbation experiments. study on the spring clear-water phase. Limnology and Oikos, 66, 193–208. Oceanography, 31, 478–490. Ramcharan C.W., McQueen D.J., Demers E., Popiel S.A., Lathrop R.C., Carpenter S.R. & Robertson D.M. (1999) Rocchi A.M., Yan N.D., Wong A.H. & Hughes K.D. Summer water clarity responses to phosphorus, (1995) A comparative approach to determining the role Daphnia grazing, and internal mixing in Lake Mendota. of fish predation in structuring limnetic ecosystems. Limnology and Oceanography, 44, 137–146. Archiv fu¨r Hydrobiologie, 133, 389–416. Lyche A., Andersen T., Christoffersen K., Hessen D.O., Reynolds C.S. (1994) The ecological basis for the success- Hansen P.H.B. & Klysner A. (1996) Mesocosm tracer ful biomanipulation of aquatic communities. Archiv fu¨r studies. 1. Zooplankton as sources and sinks in the Hydrobiologie, 130, 1–33. pelagic phosphorus cycle of a mesotrophic lake. Ripl W. (1976) Prozesssteuerung in gescha¨digten See- Limnology and Oceanography, 41, 460–474. O¨ kosystemen. Vierteljahrsschrift der Naturforschenden Mazumder A., Taylor W.D., Lean D.R.S. & McQueen D.J. Gesellschaft in Zu¨rich, 121, 301–308. (1992) Partitioning and fluxes of phosphorus: mechan- Scheffer M. (1998) Ecology of Shallow Lakes. Chapman & isms regulating the size-distribution and biomass of Hall, London, UK. plankton. Archiv fu¨r Hydrobiologie Special Issues Advances Shapiro J., Lamarra V. & Lynch M. (1975) Biomanipula- of Limnology, 35, 121–143. tion: an ecosystem approach to lake restoration. In: McQueen D.J. (1998) Freshwater food web biomanipula- Water Quality Management Through Biological Control tion: a powerful tool for water quality improvement, (Eds P.L. Brezonik & J.L. Fox), pp. 85–96. University of but maintenance is required. Lakes and Reservoirs: Florida, Gainesville. Report no. ENV-07-75-1. Research and Management, 3, 83–94. Sommer U., Gliwicz Z.M., Lampert W. & Duncan A. McQueen D.J., Post J.R. & Mills E.L. (1986) Trophic (1986) The PEG-model of seasonal succession of relationships in freshwater pelagic ecosystems. Cana- planctonic events in fresh water. Archiv fu¨r Hydrobiolo- dian Journal of Fisheries and Aquatic Sciences, 43, 1571– gie, 106, 433–471. 1581. Stenson J.A.E. (1988) Animal structure and primary McQueen D.J., Ramcharan C.W., Yan N.D., Demers E., production: An experimental study. In: Eutrophication Perez-Fuentetaja A. & Dillon P.J. (2001) The Dorset and Lake Restoration. Water Quality and Biological Impacts food web piscivore manipulation project – Part 1: (Ed. G. Balvay), pp. 161–169. Institut national deInsti- objectives, methods, the physical-chemical setting. tut de Limnologie, Thonon-les-Bains. Archiv fu¨r Hydrobiologie Special Issues Advances in Stenson J.A.E., Bohlin T., Henrikson L., Nilsson B.I., Limnology, 56, 1–21. Nyman H.G., Oscarson H.G. & Larsson P. (1978) Meijer M.-L., de Boois I., Scheffer M., Portielje R. & Effects of fish removal from a small lake. Verhandlun- Hosper H. (1999) Biomanipulation in shallow lakes in gen der Internationalen Vereinigung fu¨r Theoretische und The Netherlands: an evaluation of 18 case studies. Angewandte Limnologie, 20, 794–801. Hydrobiologia, 409, 13–30. Sterner R.W., Elser J.J. & Hessen D.O. (1992) Stoichio- Moss B. (1990) Engineering and biological approaches to metric relationships among producers, consumers and the restoration from eutrophication of shallow lakes in nutrient cycling in pelagic ecosystems. Biogeochemistry, which communities are important com- 17, 49–67. ponents. Hydrobiologia, 200 ⁄201, 367–378. Tallberg P., Horppila J., Vaisanen A. & Nurminen L. Nicholls K.H. (1999) Evidence for a trophic cascade effect (1999) Seasonal succession of phytoplankton and on north-shore western lake Erie phytoplankton prior zooplankton along a trophic gradient in a eutrophic

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295 Top-down control of phytoplankton 2295

lake – implications for food web management. Hydro- predators of Daphnia. Archiv fu¨r Hydrobiologie, 149, biologia, 412, 81–94. 177–192. Uhlmann D. (1955) Abwasserbedingte Massenent- Wright D.I. & Shapiro J. (1984) Nutrient reduction by wicklungen von Daphnia magna und Daphnia pulex. biomanipulation: an unexpected phenomenon, and Vom Wasser, 22, 167–175. its possible cause. Verhandlungen der Internationalen Vanni M.J. & Layne C.D. (1997) Nutrient recycling and Vereinigung fu¨r Theoretische und Angewandte Limnologie, herbivory as mechanisms in the ‘top-down’ effect of 22, 518–524. fish on algae in lakes. Ecology, 78, 21–40. Yiyong Z., Jianqiu L. & Yongqing F. (2000) Effects of Vanni M.J., Luecke C., Kitchell J.F., Allen Y., Temte J. & submerged macrophytes on kinetics of alkaline phos- Magnuson J.J. (1990) Effects on lower trophic levels of phatase in Lake Donghu – I. Unfiltered water and massive fish mortality. Nature, 344, 333–335. sediments. Water Research, 34, 3737–3742. Wissel B., Freier K., Mu¨ ller B., Koop J. & Benndorf J. (2000) Moderate planktivorous fish biomass stabilizes (Manuscript accepted 25 March 2002) biomanipulation by suppressing large invertebrate

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2282–2295