Freshwater Biology (2002) 47, 2453–2465

Biomanipulation of lake : successful applications and expanding complexity in the underlying science

THOMAS MEHNER,* JU¨ RGEN BENNDORF,† PETER KASPRZAK* and RAINER KOSCHEL* *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: [email protected]

2002 Blackwell Science Ltd 2453 2454 T. Mehner et al.

Keywords: heterogeneity, lakes, maintenance, management, niche shifts, nutrients

nipulation success may require more detailed under- Introduction standing of interactions within aquatic food webs. More than 10 detailed reviews on biomanipulation The results of the first international conference on have been published since 1990 (e.g. Benndorf, 1990; biomanipulation held in Amsterdam in 1989 (Gulati Hansson et al., 1998) when the proceedings of the first et al., 1990) serve as a starting point to illustrate the international meeting on the topic appeared (Gulati main topics in biomanipulation research about et al., 1990). This remarkable activity demonstrates the 12–15 years ago (Table 1). Many studies focused on continuing immense interest in this issue from both a separate trophic levels, such as and scientific and practical viewpoint. The focus of the , and their links with the trophic levels early reviews was on enclosure and laboratory adjacent to them. Some detailed attention was given to experiments. More recently, interest has shifted to species and functional groups that are indirectly elucidating responses observed after whole-lake affected by biomanipulation. In addition, the ability manipulations (Hansson et al., 1998; McQueen, 1998; of shallow lakes to switch between two alternate Drenner & Hambright, 1999). None of the reviews stable states was clearly expressed, and the limitations leaves a doubt that biomanipulation can be an of simple food-chain models to explain some of the effective and powerful tool for water quality improve- responses observed in lakes were highlighted. Finally, ment. The average success rate of food-web mani- the potential of biomanipulation for improving lake pulations is about 60% (10 of 17 case studies; Hansson water quality was assessed based on the available et al., 1998; 25 of 41 case studies; Drenner & empirical and theoretical evidence (Table 1). Hambright, 1999) and only 15% of the whole-lake Seven partially different themes were identified at biomanipulation experiments (6 of 41 studies) the second symposium on biomanipulation held in reanalyzed by Drenner & Hambright (1999) were 2000 in Rheinsberg near Berlin, Germany (Table 1). considered a definite failure. This shift in emphasis is best characterised as an effort Hansson et al. (1998) noted that most of the suc- towards a broader, more synthetic view of biomanip- cessful applications were founded essentially on ulation at the whole-lake scale. This shift was accom- simple food chain theory (Hairston, Smith & Slobod- panied by and resulted from a large number of kin, 1960) and its derivatives such as the biomanipu- whole-lake biomanipulation experiments, which lation concept (Shapiro, Lamarra & Lynch, 1975), replaced the formerly dominating small-scale two-level the trophic cascade model (Carpenter, Kitchell & experiments. Hodgson, 1985), the top-down : bottom-up theory In this review and synthesis paper, we elucidate the (McQueen, Post & Mills, 1986), and the holistic food- recent developments in the new topics in some detail web model (Persson et al., 1988). Biomanipulation by combining results from papers presented at the refers here to the deliberate reduction of planktivory, symposium in Rheinsberg and included in this special which is followed by an increase in the abundance issue, and findings from a range of other studies that and size of zooplankton (predominantly large Daphnia have been published mostly since 1990. We will point species) and results in increased grazing pressure on out the progress made during the last decade by phytoplankton and ultimately clearer water of lakes. relating our conclusions on the current state of The desired reduction of planktivory may be achieved biomanipulation research to the synthesis of the either by removing zooplanktivorous fish manually or 1989 conference (Lammens et al., 1990). by promoting an abundant piscivorous fish commu- nity by stocking and protection measures to increase The distinction between shallow and stratified lakes predation pressure on the planktivorous fish. The expectation that this simplistic approach works in all There is widespread consensus that biomanipulation situations is in contrast with the abundance of probably has a much higher success rate in shallow publications highlighting the complexity of aquatic than in stratified deep lakes (Gulati et al., 1990; food webs. This suggests that predictions of bioma- McQueen, 1998; Scheffer, 1998). The main advantage

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2453–2465 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 Topic

Edibility of phytoplankton – Quality and quantity of phytoplankton Effects of nutrient concentration on phytoplankton community structure stability Distinction between shallow and The distinction between Deepwater areas and stratified lakes shallow and stratified lakes macrophytes as refugia Role of macrophytes Alternate stable states of shallow lakes Alternate stable states of shallow lakes Indirect effects – Invertebrate predators Rotifers Benthivorous fish – phytoplankton link Biomanipulation and ecosystem Nutrient supply and recycling The effects of nutrient supply research Biomanipulation efficiency and recycling on the success Resource-quality response not threshold of P-loading of biomanipulation predicted by food-chain models Threshold of in-lake P-concentration Size–structured interactions Trophic state of the lake Stronger role of benthivorous fish Nutrient recycling by fish and zooplankton Benthivorous fish Ontogenetic niche shifts and The importance of ontogenetic size–structured trophic interactions niche shifts and size-structured Ontogenetic niche shifts in piscivores interactions Role of young-of-the-year fish Size refuges of prey against gape-limited predators Temporal and spatial heterogeneity The role of temporal variability in food webs and spatial heterogeneity Diel migrations of fish in food webs Littoral–pelagic coupling Benthic–pelagic coupling ‘Timing’ of predator–prey interactions 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 The relative proportion of planktivores ⁄ benthivores piscivores and planktivores ⁄ Role of predatory invertebrates benthivores in the fish community Balance between piscivores and planktivores and benthivores Importance of omnivory Situation in tropical water bodies

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Table 1 (Continued )

Amsterdam 1989 Rheinsberg 2000 Topic

Management Long-term maintenance of The requirement of long-term Assessment of the application biomanipulation maintenance of potential of biomanipulation Repeated stocking measures necessary biomanipulation measures Role of nutrient supply and Drastic manual fish removal required concentration Press perturbations necessary Alternative stable states of food-web configuration

Management and sustainability The management and Co-operation of all lake users sustainability aspects of Water quality and sustainable biomanipulation fisheries management of food-web manipulations in shallow lakes is the Zwemlust (the Netherlands; Van de Bund & Van potential for (re)colonisation of large bottom areas by Donk, 2002) indicate the switching of shallow lakes macrophytes, which promote the clear-water state of between the turbid and clear-water states, with drastic shallow lakes through a number of mechanisms: (1) fish removals and heavy external nutrient loading Macrophyte beds can act as a refuge for zooplankton working antagonistically. There is also a convincing from fish predation (Stansfield et al., 1997); (2) the example that stocking of piscivores without manual feeding efficiency of predatory fish such as perch removal of planktivores may shift shallow lakes into (Perca fluviatilis L.) and pike (Esox lucius L.) in the clear state. In Lake Udbyover (Denmark), perch macrophyte beds is higher than that of planktivorous and pike stocked over a 5-year period induced a or benthivorous cyprinids such as roach [Rutilus decrease in planktivorous and benthivorous fish rutilus (L.)] or bream [Abramis brama (L.)] (Winfield, density, which eventually led to the re-appearance 1986; Grimm & Backx, 1990); (3) experimental and of submerged macrophytes (Skov et al., 2002). observational results showing that high densities of phytoplankton, especially cyanobacteria, rarely occur The effects of nutrient supply and recycling when dense macrophyte beds are present suggest that on the success of biomanipulation macrophytes compete with phytoplankton success- fully for nutrients (Van Donk et al., 1990) and may It has long been proposed that bottom-up effects of excrete allelopathic substances against cyanobacteria nutrients on the structure of pelagic food webs remain (Declerck et al., 2000); (4) Conditions inside macro- effective even in strongly top-down manipulated phyte beds may increase denitrification, thus contri- lakes (e.g. McQueen et al., 1986). Benndorf (1987) buting to a decreased availability of nitrogen for suggested therefore that the reduction of nutrient phytoplankton growth (Van Donk et al., 1993); and (5) runoff from the catchment may be an important resuspension of bottom material is generally lower in prerequisite for successful biomanipulation, and that macrophyte beds (Barko & Smart, 1981). All these an annual loading threshold below 0.6–0.8 g of total ) mechanisms work together towards stabilising or Pm 2 of lake surface area must be reached before lake even enhancing water clarity, which in turn expands water quality can be improved by biomanipulation the water depth and bottom area where macrophytes (Benndorf et al., 2002). Similarly, Jeppesen et al. (1991) can grow. Recognition of this positive feedback determined an in-lake P-concentration of about ) mechanism has led to the theory of alternate stable 100 lgL 1 as the critical level below which long-term states in shallow lakes, with rapid shifts occurring effects of biomanipulation can be expected in shallow between a turbid, plankton-dominated state and a lakes. Long-term data from Feldberger Haussee, clear, macrophyte-dominated state (Scheffer, 1998). Germany, a stratified eutrophic hardwater lake, sug- Shallow lakes in the Netherlands are sensitive to gest that the improved water quality observed in that changes in bream biomass (Lammens, van Nes & lake over the past 10 years can only partly be Mooij, 2002). Similarly, long-term data from Lake attributed to biomanipulation, because the improve-

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2453–2465 Biomanipulation today – summary and review 2457 ment concurred with a decline in the nutrient loading A re-discovered effect of biomanipulation is the (Mehner et al., 2001). Increasing calcite precipitation enhancement of nutrient recycling by aquatic animals, and phosphorus coprecipitation may have further including fish, which leads to an indirect bottom-up contributed to the decline in nutrient concentrations influence on pelagic food-web structure. Many effects and, indirectly, to the reduction of phytoplankton of fish on phytoplankton that were originally attrib- biomass in that lake (Koschel, 1997). uted to the feeding of fish on zooplankton can be In contrast to the findings above, recent studies in better explained as indirect effects of nutrient excre- North America, including experiments involving tion and, in part, egestion by fish (Brabrand, Faafeng nutrient additions to lakes, appear not to support the & Nilssen, 1990; Schindler et al., 1993; but see idea that the P input rate must fall below a certain Attayde & Hansson, 2001). Reduced rates of nutrient threshold for herbivory to control phytoplankton bio- recycling resulting from a reduced biomass of mass (Carpenter et al., 2001). However, as nutrients planktivorous fish were apparently responsible for were supplied experimentally only during short dos- the success of biomanipulation in the Finnish Lake age periods, the phosphorus accumulation rate of the Vesija¨rvi. Zooplankton biomass did not increase in sediment was probably higher than under equilibrium this lake following biomanipulation (Horppila et al., conditions. Therefore, the experiments may not have 1998), suggesting that biomanipulation success was mimicked external loading well. In addition, high light mainly triggered by bottom-up forces induced by attenuation resulting from high concentrations of col- intensive fish removal. Similarly, the reduced P- ) oured DOC (up to 9.5 units m 1) inhibited the devel- recycling after a massive fish kill of the omnivorous opment of inedible phytoplankton in those experiments. Tilapia and Oreochromis in a shallow tropical reservoir The trophic state of lakes has an impact on food- contributed to a short-term improvement in water chain length, thus delineating the potential for bio- quality (Starling et al., 2002). In contrast, Tarvainen, manipulation by changes in the upper trophic levels. Sarvala & Helminen (2002) calculated that P-release Persson et al. (1992) argued that both oligotrophic and by a roach population could not directly account for eutrophic lakes in Europe possess three-level food the late summer increase in P concentration observed chains without piscivores (phytoplankton, zooplank- in the biomanipulated Lake Ko¨ylio¨nja¨rvi in Finland, ton, planktivorous fish), whereas mesotrophic lakes although young fish, which exhibit high metabolic have four levels with abundant populations of pred- rates, dominated the population. However, when atory fish, mainly perch, with a strong top-down growth rates and P demand of roach and the often influence on planktivorous roach populations. very large internal P loading from the sediment According to Persson et al. (1992), the absence of (Søndergaard, Jensen & Jeppesen, 2001) are balanced, piscivorous perch in eutrophic lakes is because of the P-recycling by fish may have a low impact on total P fact that perch is competitively inferior to roach under availability in most eutrophic lakes. the unfavourable food conditions for perch in eutro- Benthivorous fish species such as bream and phic lakes. A similar argument for stronger top-down common carp (Cyprinus carpio L.) stir up the lake control in mesotrophic lakes was derived from bottom and thus increase sediment re-suspension, experimental work on zooplankton–phytoplankton water turbidity and internal nutrient loading interactions: Carney (1990) and Elser & Goldman (Breukelaar et al., 1994). In addition, the feeding (1991) proposed the ‘mesotrophic maximum hypothe- activity of these fishes may directly destroy or uproot sis’ stating that the top-down impact on phytoplank- macrophytes, implying that benthivorous fish may ton is highest under mesotrophic conditions. In exert bottom-up effects on water quality (Tatrai & contrast, Sarnelle (1992) found that Daphnia grazing Istvanovics, 1986), and it has been suggested that the on phytoplankton increased with phosphorus removal of benthivorous fish determines the outcome concentration, indicating that the lakes most heavily of biomanipulation in shallow lakes more strongly impacted by nutrient inputs would show the greatest than the removal of planktivorous fish (Lammens response to a reduction in planktivory. Thus, the et al., 1990; Drenner & Hambright, 1999). The removal hypotheses above predict that the effectiveness of of cyprinids from Lake Ringsjo¨n, Sweden, resulted in biomanipulation measures may differ systematically a rapid change in the diversity of benthic inverte- with the trophic state of lakes. brates, indicating that these fish did indeed disturb

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2453–2465 2458 T. Mehner et al. the lake bottom, with possible implications for pelagic smaller daphnids after hatching than during later nutrient concentrations and the food web (Svensson, growth stages (Schael, Rudstam & Post, 1991). How- Bergman & Andersson, 1999). ever, strong demographic effects in Daphnia popula- tions would only occur when fish feed preferentially on mature, egg-bearing daphnids (Mehner, 2000). In The importance of ontogenetic niche shifts addition, it is likely that the midsummer decline of and size-structured interactions daphnids is caused by many interacting mechanisms, Body size of organisms is important for determining including predation by (young) fish and predatory the shape and strength of trophic interactions, invertebrates as well as natural senescence and death particularly in aquatic habitats where size-structured (Benndorf et al., 2001; Hu¨ lsmann & Voigt, 2002). fish populations dominate (Werner & Gilliam, 1984). Another mechanism relating to the size-structure of Because single species may show shifts in diet or fish communities is the interaction between piscivores habitat use during ontogeny, different developmental and their prey. If prey fish can grow to a sufficiently stages must be treated separately when such interac- large size, they reach a refuge against being fed by tions are analysed. Evidence of ontogenetic niches predators (Hambright, 1994; Persson & Eklo¨v, 1995), comes from fish communities in both North America because strong predation may shift the age structure (Werner, 1992) and Europe (Persson, 1994). Of of prey populations towards larger individuals particular interest for biomanipulation is the diet shift (Bro¨nmark et al., 1995), preventing the top-down of fish that start their life as planktivores but shift to control of large planktivores by piscivores (Lammens, piscivory when reaching a certain length (e.g. perch 1999). As a result, planktivorous species such as and pikeperch, Sander lucioperca (L.); Persson, common bream or roach can be preyed upon only at Bystro¨m & Wahlstro¨m, 2000; Beeck et al., 2002). younger stages. Establishing a top trophic level of piscivores with The shift from edible to inedible phytoplankton these species therefore entails enhanced planktivory species observed during biomanipulation in response by the young (Mehner et al., 1996). In addition, as the to intense grazing by daphnids is another negative abundance of adult planktivorous fishes decreases, feedback mechanism in foodwebs relating to size- competition for food diminishes, which favours the structure. To overcome this problem, stocking lakes recruitment of young stages (Romare & Bergman, with fish such as silver carp [Hypophthalmichthys 1999). As a result, young-of-the-year (YOY) fish often molitrix (Val.)], which are capable of feeding on increase greatly after several years of biomanipulation phytoplankton, has been suggested (Starling et al., (Mehner et al., 1996). As these small fish have higher 1998). However, as these fish also suppress daphnids, biomass-specific food requirements and occur in high their stocking is recommended only in geographical densities, their predation impact on zooplankton is regions where daphnids are naturally absent (Radke higher than that of the same biomass of adult & Kahl, 2002). planktivorous fish (Romare & Bergman, 1999). The strong predation impact is particularly detrimental for The role of temporal variability and spatial heterogeneity water quality during the summer months (Romare, in food webs Bergman & Hansson, 1999). It has been hypothesised, in particular, that feeding by YOY fish may cause the The differing temporal or spatial scales on which most commonly observed phenomenon of midsummer trophic interactions in lakes occur have received decline in Daphnia abundance, which is often accom- relatively little attention. The intensity of fish– panied by reduced water transparency resulting from zooplankton interactions may vary along spatial gra- high phytoplankton biomass, although quantitative dients in lakes (George & Winfield, 2000). The potential evidence for this mechanism is limited (Luecke et al., growth rate of piscivores depends on the spatial 1990; Mehner et al., 1998). Quantitative impacts of distribution of their prey fish (Mason & Brandt, 1996). YOY fish on zooplankton may have rarely been The predation impact by piscivorous perch and pike- demonstrated because trophic interactions between perch on their own YOY descendants varied between YOY fish and zooplankton also depend on size littoral and pelagic areas (Do¨rner, Wagner & Benndorf, relationships: Fish are gape-limited and thus ingest 1999), and planktivorous YOY fish influenced daph-

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2453–2465 Biomanipulation today – summary and review 2459 nids more strongly in littoral than in pelagic areas in ited by invertebrate predators such as Chaoborus, the stratified hypertrophic Bautzen Reservoir Daphnia may be ‘squeezed’ and threatened by (Hu¨ lsmann et al., 1999). A structural difference of the predation from both vertebrates in the epilimnion trophic cascade within and outside of submerged and invertebrates in the hypolimnion. Dawidowicz macrophytes stands has been found in shallow lakes, et al. (2002) concluded that this dual predation resulting in a higher water transparency within macr- pressure may have been responsible for the extinc- ophyte beds (Schriver et al., 1995). However, it is not tion of the large Daphnia hyalina Leydig during clear whether mechanisms acting strongly in one biomanipulation of the deep Lake Mutek in Poland, particular habitat have a significant impact on the whereas smaller cladocerans responded positively to strength of interactions at the whole-lake scale. the declining fish abundance. Planktivorous fish seeking daytime shelter from Temporal scales are also important to consider, predation by piscivorous fish or birds either in the because generation times of different members of deep hypolimnion or in littoral vegetation may lead to pelagic food webs differ widely (Ramcharan et al., a reduction of predatory losses in pelagic zooplankton 1995). Life spans may range from days for phyto- (Gliwicz & Dawidowicz, 2001). Consequently, stock- plankton to > 20 years for piscivorous fish. In Lake ing with visually oriented pelagic piscivores such as Mendota, U.S.A., the impacts of a massive natural die- the strongly day-active perch (Jacobsen et al., 2002) off of a strong cisco (Coregonus artedi Lesueur) year might induce a behaviourally mediated biomanipula- class on plankton community structure and water tion effect by preventing the daytime feeding of clarity were detectable for a decade (Lathrop et al., planktivores on daphnids in the open water. A similar 2002). Yodzis (1988) suggested that evaluation of the effect can be obtained by adding fish kairomones to long-term dynamics of whole-lake experiments has to the water (Gliwicz, 2002). In addition, planktivory can consider time scales twice the sum of the life spans of be further suppressed by the presence of pelagic all members of the trophic chain, that is at least predators such as pikeperch, which are active over the 50 years in most lakes. Such long observations fol- whole diurnal cycle (Brabrand & Faafeng, 1993; lowing biomanipulation experiments have not yet Ho¨lker et al., 2002). been made. Coupling of the dynamics of organisms A similar spatial coupling occurs if fish feed in one differing greatly in regard to generation times may be area of a lake and excrete in another area. In this apparent only over longer time scales, not over a few way, fish may subsidise the pelagic nutrient pool by months or seasons (Persson et al., 1992). feeding in nearshore areas and then migrating to the Time scale considerations also relate to the issue of central open-water region (littoral-pelagic coupling) trophic level control by either predation or resource or by feeding at the lake bottom and subsequently limitation. Gliwicz (2002) pointed out that only the moving upwards into the water column (benthic- bottom-up control is mediated by time-dependent pelagic coupling). In both cases, new nutrients are parameters such as the individual growth rate, the supplied to pelagic phytoplankton in a directly reproduction rate, and the population growth rate. usable form. Restriction of this fish-mediated nutrient Top-down control, in contrast, acts on state variables transfer in some cases was found to be more such as biomass, individual body size, and population important for the success of biomanipulation than density, independent of the rate at which these the release of feeding pressure on zooplankton entities are produced. following removal of planktivorous fish (Horppila Consideration of temporal scales was found to be et al., 1998). crucial also for understanding the initiation of the Consideration of habitat diversity is important midsummer decline of daphnids, where the relative also if the physical or chemical characteristics of a timing of all processes involved (predation, food water body create spatial refuges that affect the supply, ageing) determines whether the decline in strength of trophic interactions. For example, layers Daphnia density at the end of spring eventually with reduced oxygen concentrations may help daph- results in a longer or shorter period in midsummer nids escape fish predation because fish often avoid with extremely low Daphnia abundance (Post & these zones (Wright & Shapiro, 1990; Jeppesen et al., Kitchell, 1997; Benndorf et al., 2001; Hu¨ lsmann & 1997). However, if the anoxic hypolimnion is inhab- Voigt, 2002).

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2453–2465 2460 T. Mehner et al. Even repeated stocking of piscivores may not be The relative proportion of piscivores sufficient without manual removal of planktivores. and planktivores ⁄benthivores in the fish community Biomanipulation by piscivore stocking had the lowest As biomanipulation requires drastic removal of success rate among a range of measures evaluated by planktivorous fish, the question may arise why not Drenner & Hambright (1999). Similarly, in the create a fish community composed of piscivores only? stratified Feldberger Haussee, the continuous removal Intentional changes of both the piscivorous and of planktivores by low-intensity fishing did not result planktivorous levels in a whole-lake biomanipulation in a long-term decline of the planktivorous fish stock experiment have indicated that the goal of removing and did not greatly enhance crustacean biomass the planktivorous level from a lake totally may be (Kasprzak et al., 1993; Mehner et al., 2001). In contrast, impossible to achieve in practice (Wissel et al., 2000). drastic and fast removal of > 75% of the planktivores Moreover, total removal of planktivorous fish would within one season (Meijer et al., 1999) has been leave the planktivore niche unoccupied, allowing recommended as a measure to shift shallow lakes to other groups that prey on daphnids, such as predat- the clear-water state (Hansson et al., 1998). Some ory invertebrates (Wissel et al., 2000), to invade and critical (Barthelmes, 1988) or optimal (Benndorf, fill the gap. 1990) absolute densities of planktivorous fish may be If planktivorous fish cannot and should not be an even better endpoint for fish reductions than the completely removed from biomanipulated lakes, what relative removal rates suggested by Meijer et al. (1999) is the most appropriate balance between planktivores and others. It is not yet clear, however, whether such and piscivores? Besides the generally desired high critical fish densities are lake-specific or can be species diversity and length variability of the pisci- generally defined. Given that even shallow lakes vore stock (Benndorf, 1990; Perrow et al., 1997), may show little sign of long-term stability of bioma- Benndorf & Kamjunke (1999) recommended a propor- nipulation effects (Perrow et al., 1999), repeated fish tion of 30–40% piscivores. This recommendation is stock reductions have been proposed as a simple and based on experimental evidence from long-term bio- cost-effective management strategy as long as external manipulations in German lakes showing that bioma- nutrient supplies have not been markedly reduced nipulation is successful when the fish community (Van De Bund & Van Donk, 2002). consists of >20–25% (Feldberger Haussee; Wysujack The drastic reductions in planktivore fish stocks & Mehner, 2002) and up to 50% piscivores (Bautzen normally required for successful biomanipulation Reservoir; J. Benndorf & H. Do¨rner, unpublished indicate that press perturbations are required to shift data). Detailed energetic balances supporting these a system into another state; the impact of pulsed empirical values are currently lacking, however. perturbations appears to be too small (Persson et al., 1993). This conclusion may hold particularly true if alternative stable states of food web configurations The requirement of long-term maintenance exist, as has been proposed for shallow lakes of biomanipulation measures (Scheffer, 1998). However, there is no evidence at Biomanipulation probably does not lead to stable food present that alternative stable states also occur in web configurations and therefore requires continuous stratified lakes (Persson, 1994; Benndorf et al., 2002), efforts to suppress planktivores (Kitchell, 1992; indicating that only repeated press perturbations may McQueen, 1998). For example, the increased recruit- hold stratified lakes in the desired food-web structure. ment success of planktivores following a period of planktivorous fish removals, requires control by either The management and sustainability aspects piscivores or repeated manual removal (Romare & of biomanipulation Bergman, 1999; Van de Bund & Van Donk, 2002). Moreover, planktivorous fish may rapidly invade Biomanipulation is used to improve the water quality biomanipulated lakes, particularly if the lakes are of lakes, and many of the studies documented in connected to other water bodies. Prevention of immi- literature were initiated because of the practical gration may be especially complicated if the connec- requirement of lake restoration rather than scientific tions are used for navigation (Perrow et al., 1997). interest (Carpenter & Kitchell, 1992). Therefore, in

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2453–2465 Biomanipulation today – summary and review 2461 many biomanipulations, the co-operation of lake and groups play a central role in biomanipulation. The fishery managers, anglers and scientists was part of scientific data and expertise obtained in biomanipu- the planning and manipulation phases (e.g. Benndorf, lation experiments in a range of lake types serve as 1990; Kitchell, 1992; Lathrop et al., 2002). In addition, the basis for designing appropriate fish manipulation success was often reported in those cases where measures in particular water bodies, and for fine- authorities and lake users supported the biomanipu- tuning ongoing biomanipulations. In contrast to the lation (Horppila et al., 1998; Perrow et al., 1999). situation 10–15 years ago, quantitative approaches to Guidelines for biomanipulating lakes have been assess the top-down and bottom-up effects of fish are developed (Moss, Madgwick & Phillips, 1996; increasingly used (bioenergetics, individual-based Benndorf & Kamjunke, 1999) and the combination of modelling). The importance of young-of-the-year water quality management and sustainable fisheries fish, often neglected in earlier studies, is now fully management by biomanipulation has received acknowledged as these fish are the dominant increasing attention during the last years (Lammens, zooplankton feeders in many lakes. 1999; Wysujack et al., 2001), particularly in North 2. The confounding role of nutrients in determining America and parts of Europe where fisheries favour the potential for successful biomanipulations is now piscivorous species as catch. For example, in Lake clearer. The thresholds for nutrient supply and con- Mendota, U.S.A., size and bag limits imposed on centrations in lakes suggested in earlier studies have recreational fishermen were one of the most important been confirmed by, and more precisely described in, restrictions to support biomanipulation, which in turn recent studies. In combination with conclusion 1, this enabled the anglers to catch larger specimens than affirmation is a partial revival of the top-down : bot- before (Lathrop et al., 2002). In addition, during recent tom-up concept by McQueen et al. (1986), which years, increasing interest in catching living bream for predicts the strongest effect of biomanipulation on stocking of angling waters allows Dutch fishermen to pelagic food webs when both fish and nutrients are obtain income by combining the desired decline in altered. bream stocks with the effect of enhanced water 3. The scientific background of biomanipulation, transparency (Lammens et al., 2002). Even in tropical lake food-web ecology, has become even more countries there is potential to support water-quality complex than was conceived after the 1989 confer- goals by stocking with piscivores and controlled ence. The consideration of scales is important for fishery. Evidence from a reservoir in tropical Brazil understanding trophic interactions along the tem- suggests that dense populations of omnivorous tila- poral (diel, seasonal, interannual), spatial (habitat pias increase nutrient concentrations and promote coupling, lake and catchment relationships), and algal blooms as a result of P-recycling and bioturba- interorganismic (size structure, ontogeny) axes. tion. Therefore, a professional tilapia cast-net fishery Besides scales, boundary conditions such as lake has been established to control the population density depth, underwater light climate, temperature of fish and thus limit the occurrence of cyanobacterial regime, mixing intensity and trophic state govern blooms and fish kills, in addition to generating income the response of complex food webs to changes in for the local fishermen (Starling et al., 2002). predation strength. Thus, simple food-chain models cannot be realistically assumed to reflect the multi- tude of possible effects of biomanipulations, Conclusion although they can mirror major food-web changes A generally better understanding of the complexity of in response to press perturbations. However, for the lake food webs and the frequent application of fine-tuning of ongoing and for predicting success of biomanipulation as a lake restoration technique have future biomanipulations, detailed insights into the emerged from the recent developments in biomani- trophic interactions within pelagic food webs are pulation research, as compared with the findings until necessary. 1989 (Table 1). The main progress can be summarised 4. Biomanipulation can be regarded as an approach as follows: to water quality improvement that requires the 1. Interactions between piscivorous, planktivorous combination of research and management. Most lake and benthivorous fish and their respective prey managers currently learn by doing, using biomanip-

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2453–2465 2462 T. Mehner et al. ulation as an adaptive management strategy. There is Benndorf J., Kranich J., Mehner T. & Wagner A. (2001) some agreement between fisheries and water quality Temperature impact on the midsummer decline management with respect to the goals of biomanip- of Daphnia galeata: an analysis of long-term data from ulation and ways to achieve these goals. Therefore, the biomanipulated Bautzen Reservoir (Germany). even if biomanipulation ends up as a failure in some Freshwater Biology, 46, 199–211. Brabrand A. & Faafeng B. (1993) Habitat shift in roach water bodies, advantages for some lake users may (Rutilus rutilus) induced by pikeperch (Stizostedion ensue. Furthermore, sound scientific knowledge on lucioperca) introduction: predation risk versus pelagic the behaviour of aquatic ecosystems can only be behaviour. Oecologia, 95, 38–46. obtained by manipulating systems of adequate size Brabrand A., Faafeng B.A. & Nilssen J.P.M. (1990) over long periods (e.g. Carpenter, 1996). As this type Relative importance of phosphorus supply to phyto- of research is not easily funded in most countries, the plankton production: fish excretion versus external results from public lake management programmes loading. Canadian Journal of Fisheries and Aquatic can help collecting the necessary data. Sciences, 47, 364–372. Breukelaar A.W., Lammens E.H.R.R., Breteler J.G.P.K. & Tatrai I. (1994) Effects of benthivorous bream (Abramis Acknowledgments brama) and carp (Cyprinus carpio) on sediment resus- We are grateful to E. van Donk, R. Drenner, L.-A. pension and concentrations of nutrients and chloro- phyll a. Freshwater Biology, 32, 113–121. Hansson, E. Jeppesen, L. Persson, L.G. Rudstam, M. Bro¨nmark C., Paszkowski C.A., Tonn W.M. & Hargeby Gessner, and an anonymous referee for constructive A. (1995) Predation as a determinant of size structure suggestions. in populations of crucian carp (Carassius carassius) and tench (Tinca tinca). Ecology of Freshwater Fish, 4, 85–92. References Carney H.J. (1990) A general hypothesis for the strength of food web interactions in relation to trophic state. Attayde J.L. & Hansson L.-A. (2001) The relative Verhandlungen der Internationalen Vereinigung fu¨r Lim- importance of fish predation and excretion effects on nologie, 24, 487–492. planktonic communities. Limnology and Oceanography, Carpenter S.R. (1996) Microcosm experiments have 46, 1001–1012. limited relevance for community and ecosystem ecol- Barko J.W. & Smart R.M. (1981) Sediment-based nutrition ogy. Ecology, 77, 677–680. of submersed macrophytes. Aquatic Botany, 10, 339–352. Carpenter S.R., Cole J.J., Hodgson J.R., Kitchell J.F., Pace Barthelmes D. (1988) Fish predation and resource reac- M.L., Bade D., Cottingham K.L., Essington T.E., tion: biomanipulation background data from fisheries Houser J.N. & Schindler D.E. (2001) Trophic cascades, research. Limnologica, 19, 51–59. nutrients, and lake productivity: whole-lake experi- Beeck P., Tauber S., Kiel S. & Borcherding J. (2002) 0+ ments. Ecological Monographs, 71, 163–186. perch predation on 0+ bream: a case study in a Carpenter S.R. & Kitchell J.F. (1992) Trophic cascade and eutrophic gravel pit lake. Freshwater Biology, 47, 2359– biomanipulation: interface of research and manage- 2369. ment – a reply to the comment by DeMelo et al. Benndorf J. (1987) Food web manipulation without Limnology and Oceanography, 37, 208–213. nutrient control: a useful strategy in lake restoration? Carpenter S.R., Kitchell J.F. & Hodgson J.R. (1985) Schweizerische Zeitschrift fu¨r Hydrologie, 49, 237–248. Cascading trophic interactions and lake productivity. Benndorf J. (1990) Conditions for effective biomanipula- Bioscience, 35, 634–639. tion; conclusions derived from whole-lake experiments Dawidowicz P., Prejs A., Engelmayer A., Martyniak A., in Europe. Hydrobiologia, 200 ⁄201, 187–203. Kozlowski J., Kufel L. & Paradowska M. (2002) Benndorf J., Bo¨ing W., Koop J. & Neubauer I. (2002) Top- Hypolimnetic anoxia hampers top-down food-web down control of phytoplankton: the role of time scale, manipulation in a eutrophic lake. Freshwater Biology lake depth and trophic state. Freshwater Biology, 47, 47, 2401–2409. 2282–2295. Declerck S., DeMeester L., De Smedt P., Rommens W., Benndorf J. & Kamjunke N. (1999) Anwenderrichtlinie Vyverman W., Geenens V., Van Wichelen J., Degans H. Biomanipulation am Beispiel der Talsperre Bautzen. & Decleer K. (2000) Clear water and charophytes in a Sa¨chsisches Landesamt fu¨r Umwelt und Geologie, 19 pp. hypertrophic pond. Verhandlungen der Internationalen Eigenverlag, Dresden. Vereinigung fu¨r Limnologie, 27, 541.

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