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Biomanipulation of Lake Ecosystems: Successful Applications and Expanding Complexity in the Underlying Science

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Biomanipulation of Lake Ecosystems: Successful Applications and Expanding Complexity in the Underlying Science Freshwater Biology (2002) 47, 2453–2465 Biomanipulation of lake ecosystems: 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] Ó 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 phytoplankton and scientific and practical viewpoint. The focus of the zooplankton, 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 Ó 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 Ecosystem 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
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