Freshwater Biology (2002) 47, 2282–2295
Top-down control of phytoplankton: 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 zooplankton 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