Short-Term and Long-Term Effects of Zooplanktivorous Fish Removal in A

Freshwater Biology (2002) 47, 2380–2387

Short-term and long-term effects of zooplanktivorous ﬁsh removal in a shallow lake: a synthesis of 15 years of data from Lake Zwemlust

WOUTER J. VAN DE BUND* and ELLEN VAN DONK NIOO Center for Limnology, Rijksstraatweg, Nieuwersluis, The Netherlands *Present address: European Commission, Joint Research Centre, Institute for Environment and Sustainability, T.P. 290, 21020 Ispra (Varese), Italy.

SUMMARY 1. Removal of zooplanktivorous fish (mainly bream) in 1987 from a shallow eutrophic lake in the Netherlands, Lake Zwemlust, resulted in a quick switch from a turbid state with cyanobacteria blooms to a clear state dominated by macrophytes. 2. The clear state was not stable in the long term, however, because of high nutrient loadings. 3. In 1999, another removal of zooplanktivorous fish (mainly rudd) had similar effects as in 1987, although macrophytes returned more slowly. 4. In the years directly following both interventions there was a ‘transition period’ of very clear water with high densities of zooplanktonic grazers in the absence of macrophytes; low oxygen concentrations indicate that during those years primary production was low relative to heterotrophic activity. 5. The transition period appears to provide the light climate necessary for the return of macrophytes. 6. Reduction of nutrient loading is necessary to improve water quality in Lake Zwemlust in the long term. In the short term, repeated fish stock reduction is a reasonable management strategy to keep Lake Zwemlust clear.

Keywords: alternative stable states, biomanipulation, food web interactions, lake management, macrophytes

situations depends upon many factors, including Introduction lake morphology (Benndorf, 1995), nutrient loading The relation between nutrient availability and phyto- (Hosper, 1998; Jeppesen et al., 1999), climate (Jayaweera plankton biomass in shallow lakes is not straightfor- & Asaeda, 1995), and food web structure (Klinge, ward, because the relative importance of top-down Grimm & Hosper, 1995). The concept of multiple and bottom-up controls can vary widely between both stable states in shallow lakes (Scheffer et al., 1993) has lakes and years (Jeppesen et al., 1997). Positive feed- proved to be very useful for water quality manage- back mechanisms that tend to stabilise either a clear, ment. Many lake restoration projects have demon- macrophyte-dominated state, or a turbid state char- strated the possibility to induce a switch in shallow acterised by algal blooms have been identiﬁed within lakes from the turbid to the clear state by food web a certain range of nutrient conditions (Timms & Moss, manipulation (see reviews by Perrow et al., 1997; 1984; Scheffer et al., 1993). The stability of both Hansson et al., 1998). The presence of macrophytes is usually the key Correspondence: Wouter J. Van de Bund, NIOO Center for factor stabilising the clear state in the long term (Van Limnology, Rijksstraatweg 6, 3631AC Nieuwersluis, The Donk et al., 1993). Macrophytes are considered super- Netherlands. E-mail: [email protected] ior competitors for nutrients compared with algae

2380 2002 Blackwell Science Ltd Biomanipulation of Lake Zwemlust 2381 (Kufel & Ozimek, 1994). In contrast to phytoplankton, (Secchi depth 0.3 m). Detailed descriptions of the many macrophytes may access nutrients in the limnology of the lake, before and after the first sediment (Barko & James, 1998), and increased biomanipulation in 1987, are given in Van Donk et al. denitrification in macrophyte beds may impose an (1990a, 1993) and Van Donk & Gulati (1995). additional constraint on algal growth (Meijer et al., 1994). Zooplankton grazing on phytoplankton is also Interventions enhanced within macrophyte beds, because macrophytes offer the grazers shelter from planktivorous In March 1987, the lake was drained within four days fish (Timms & Moss, 1984). Finally, allelopathic by pumping out the water. The whole fish community, substances released by macrophytes can have a weighing c. 1000–1500 kg and comprising about 75% negative impact on phytoplankton, although the bream (Abramis brama L), was removed by seine and ecological significance of this mechanism is still electrofishing. It was anticipated that fish would unclear (reviewed by Van Donk & Van de Bund, eventually recolonise the fishless lake, for example as 2002). Stabilisation of the sediment caused by the egg-material transported by birds. Therefore, it was presence of macrophyte beds additionally contributes decided to create and maintain an abundant 0+ pike to clear water (Barko & James, 1998). population. After the lake got refilled by seepage The most difficult part in the restoration of shallow (c. 3 days), it was restocked with 1600 artificially lakes usually is not to induce a switch to clear water, propagated 0+ pike (Esox lucius L) measuring 4 cm and but to maintain the clear state in the long term. In many with 140 rudds (Scardinius erythrophthalmus L) meas- cases, lakes returned to the turbid state within a few uring 9–13 cm fork length. The introduced rudd had years after food web manipulation, especially when well developed gonads. The offspring was meant to nutrient loadings remained high (Jeppesen et al., 1997). serve as food for pike. Small plants of Chara globularis The Dutch Lake Zwemlust is a good example of an (Thuill.) and 200 rhizomes of Nuphar lutea (L) were initially successful food web manipulation (Van Donk introduced. A total of 170 stacks of willow twigs were & Gulati, 1995; Van Donk, 1998), where the macro- fixed to the bottom to provide refuge and spawning phyte-dominated state was unstable in the long term. grounds for pike and as shelter for zooplankton (for In this paper we summarize the developments in further details see Van Donk et al., 1990a). Lake Zwemlust in the period 1986–2000. This period Because the water quality in the lake deteriorated includes two biomanipulations, in 1987 and 1999. Our again in the late 1990s (see Results section), it was objectives are (i) to identify the main factors respon- decided to undertake another biomanipulation in late sible for the return of the lake to the turbid state April 1999. The intention was to drain the lake again following the first intervention by analyzing long-term completely and to remove all fish. However, because monitoring data (2) to evaluate the short-term effects of logistical problems, it was only possible to lower of food web manipulation by comparing the response the water level by c. 1 m. As much of the fish stock as of key variables to the two interventions, and (3) to possible was removed by seine fishing. The total make recommendations for management strategies for removed biomass was about 150 kg, comprising Lake Zwemlust and comparable small lakes. almost exclusively rudd. None of the additional measures taken in 1987 were repeated in 1999.

Methods Monitoring data Study area The developments in Lake Zwemlust have been Lake Zwemlust is a small water body (area 1.5 ha; monitored from 1986 onwards. The sampling fre- mean depth 1.5 m), situated in the middle of the quency for determining water chemical parameters, Netherlands. It receives high external P and N loadings Secchi depth, chlorophyll-a concentration, and ) ) ) ) estimated at about 2 g P m 2 y 1 and 9 g N m 2 y 1,by zooplankton and phytoplankton composition varied seepage from the River Vecht running about 50 m from between seasons and years, but samples were taken at the lake. Before the biomanipulation in 1987, phyto- least monthly. The methods are described in detail in plankton blooms were observed throughout the year Van Donk, Gulati & Grimm (1990b) and Van Donk

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387 2382 W.J. Van De Bund and E. Van Donk ) et al. (1993). Fish biomass and composition were deter- ophyll-a concentrations up to 250 lgL 1. In summer, mined at about yearly intervals in autumn using a the phytoplankton was dominated by cyanobacteria. modified mark-recapture method by Peterson (Ricker, Macrophytes were totally absent. After the interven- 1975; Meijer et al., 1995). No fish data are available for tions, the water became clear almost immediately. the years 1994, 1996 and 1997. In 1998, fish biomass Secchi disc measurements showed almost continuous was estimated indirectly using data from the 1999 bottom sight during the period 1988–91 (Fig. 1a). sampling and the removed fish biomass during Chlorophyll-a concentrations were relatively low biomanipulation. Abundance of herbivorous and (Fig. 1b). Cyanobacteria were almost absent during omnivorous waterfowl was recorded at each sampling those years, whereas cryptophytes were relatively occasion. Biomass and composition of submerged abundant (Fig. 2). From 1992 to 1995, alternations of macrophytes in the lake were estimated yearly in late periods with clear and turbid water occurred within summer; a detailed description of the methods is the same year, and cyanobacterial blooms started to given in Ozimek, Gulati & Van Donk (1990). reoccur. A detailed analysis of changes in phytoplankton composition is presented in Romo et al. (1996). The situation deteriorated further from 1996 to 1998; at Results the end of that period, the situation was similar to the situation immediately before the biomanipulation in Long-term developments 1987. The second intervention in 1999 resulted again in Before the interventions of 1987, the lake was char- a striking increase of water transparency, similar to the acterised by very low water transparency with chlor- one observed in 1987 (Fig. 1a).

Fig. 1 Secchi depth (a), Chlorophyll-a (b), inorganic phosphorus (c) and nitrate (d) concentrations in Lake Zwemlust in 1986–2000. Dashed lines show the dates of ﬁsh removal.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387 Biomanipulation of Lake Zwemlust 2383

(a)

(b)

(c)

(d)

(e) Phytoplankton composition (Percentage of total abundance)

(f) )

Fig. 2 Phytoplankton and zooplankton in –1 (g) Lake Zwemlust in 1986–2000. Phyto- plankton panels show the contribution of cyanobacteria (a), green algae (b), diatoms (ind. L (h) (c), cryptophytes (d), and other algae (e) to total phytoplankton abundance. Zooplankton panels show the abundance Zooplankton density of large (>500 lm) crustacean zooplankton (f), small (<500 lm) crustacean zooplankton (g), and rotifers (h). Dashed lines show the dates of ﬁsh removal.

Inorganic nutrient levels showed a rather consistent cladocerans became extremely abundant during most seasonal pattern throughout the observation period, of the year, coinciding with high chlorophyll concen- with no obvious effect of the interventions. Soluble trations (Fig. 1b). Very soon after the intervention in reactive phosphorus (SRP) concentrations were con- 1999, large cladocerans (mainly D. magna) returned, ) tinuously very high (>0.2 mg L 1); there appears to be and the smaller taxa almost disappeared again. a slight tendency to decreasing SRP concentrations Rotifer densities (Fig. 2h) were rather low in the years during the period 1993–99 (Fig. 1c). Nitrate concen- following the biomanipulation in 1987, but became trations were always high during winter, with a steep more abundant in the years 1994–99. decrease in the spring (Fig. 1d) towards concentra- Macrophytes were initially absent, but appeared tions limiting algal growth (Van Donk et al., 1993). very quickly after the intervention in 1987 (Fig. 3). The Zooplankton abundance and composition show a plants reached a peak biomass of 170 g dry ) clear long-term development (Fig. 2). In the years weight m 2 in 1989. From 1989 to 1993, their biomass following the biomanipulation of 1987, the zooplank- declined, followed by two additional years character- ton was dominated by large species (mainly Daphnia ised by a high biomass. In 1996, the macrophyte magna Straus.), with rather high densities during biomass eventually decreased to very low levels and ) spring and summer (up to c. 500 ind L 1). In 1990, by 1998 had declined to zero. There was a clear small taxa (Ceriodaphnia spp., Bosmina spp.) appeared, succession of macrophyte taxa (Fig. 3). Initially the initially at very low densities. From 1990 to 1993, large plant biomass was dominated by Elodea nuttallii and small taxa were both abundant. From 1995 to (Planchon). From 1990 to 1991, Ceratophyllum demer- 1999, large cladocerans were almost absent, and small sum (L) became dominant, followed by 3 years of

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Fig. 3 Macrophyte biomass and coot density in Lake Zwemlust Fig. 4 Macrophyte and total estimated rudd biomass in Lake in 1986–98. E.n.: Elodea nuttallii; P.b.: Potamogeton berchtoldii; Zwemlust in 1986–98. E.n.: Elodea nuttallii; P.b.: Potamogeton C.d.: Ceratophyllum demersumi. berchtoldii; C.d.: Ceratophyllum demersum. The rudd biomass in 1998 was estimated from gill-net catches and removed fish biomass in 1999. Potamogeton berchtoldii (Fieb.) dominance. In 1995, Elodea returned briefly, reaching a biomass as high as that in 1989, but then declined quickly. Short-term effects of fish removal The macrophytes in Lake Zwemlust attracted high numbers of grazing birds, mainly coots (Fulica atra This section provides a more detailed comparison of L.; Fig. 3). However, coots did not appear during the short-term responses to the biomanipulations in the first years after macrophyte recolonisation, but 1987 and 1999. Water transparency (Fig. 1b) and only in 1989, when the macrophytes had already chlorophyll-a concentration (Fig. 1a) showed quite reached a high biomass (Fig. 3). Coots were especi- similar responses in both years. The lake water only ally abundant in 1989–91 and in 1995–97. These cleared up about 2 months after the lake had filled were all years in which the macrophyte biomass again. A spring bloom of green algae occurred 1 year was dominated by Elodea or Ceratophyllum. In the after the intervention in 1987, whereas no algal bloom Potamogeton-dominated years 1992–94, coots were was recorded in the spring following the 1999 inter- almost absent. vention (Fig. 1). Cyanobacteria were completely absent In 1986, the fish biomass in Lake Zwemlust was (1987) or only present at extremely low biomass levels extremely high and dominated by bream (Van Donk (1999) in the two summers following the interventions. et al., 1990b). The removal of bream in 1987 was In 1987, macrophytes returned in the very year of successful; until the end of the sampling period in biomanipulation, increasing to a biomass of as high as ) 2000, the species was never found again. Rudd, 100 g dry weight m 2 in 1988 (Fig. 3). In 1999, the which was stocked to the lake in 1987, became the response was quite different: Even in the summer of dominant fish species. The rudd population increased 2000, macrophytes were still almost absent, in spite of greatly from 1987 to 1990, reaching an estimated extremely clear water. However, a layer of filamen- ) maximum biomass of 550 kg ha 1 (Fig. 4). In subse- tous algae covered the sediment surface of the lake quent years, the biomass remained rather constant at during most of the summer. By the end of the summer this level, at least until 1995. No fish data are of 2000, the cover of filamentous algae diminished, available for the years 1994, 1996 and 1997 and the and macrophytes (mainly Potamogeton and Ceratophyl- results of the 1998 fish sampling are not reliable, lum) started to reappear. because too few marked fish were recaptured. The composition of the zooplankton community However, based on the 1999 fish sampling and the was very similar following the interventions in 1987 removed fish biomass during the biomanipulation, and 1999. Densities of large cladocerans were relat- we estimate that rudd biomass before 1999 was at ively high throughout the season (Fig. 2f), while small ) least 200 kg ha 1, excluding young of the year. These cladocerans (Fig. 2g) and rotifers (Fig. 2h) were vir- data suggest that the fish biomass had declined tually absent. considerably during the years of phytoplankton Oxygen depletion occurred following both inter- dominance (1996–98). ventions (Fig. 5). Concentrations decreased to

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Fig. 6 Succession of developmental stages in lake Zwemlust in response to biomanipulation. A: turbid state; B: transition state; C: clear state; D: clear ⁄ turbid state (see text for explanation).

Fig. 5 Oxygen concentrations in Lake Zwemlust before and after the biomanipulations in 1987 (a) and 1999 (b). Dashed lines show the dates of fish removal. distinguished. The turbid (A) and clear (C) states are separated by two transition periods – the ‘transition state’ (B) directly following the biomanipulation, and ) <3 mg L 1 in the 2 months following the refilling of the ‘clear ⁄turbid state’ (D) following the clear state. the lake. This decline was only observed during the Biomanipulation appears to induce the ‘transition two postbiomanipulation years, whereas in all other state’ (B), where the water is very clear but macro- years oxygen concentrations were near saturation phytes are absent or very rare. This ‘transition state’ is levels throughout the year. Oxygen depletion was further characterised by high densities of large daph- more severe in 1999 than in 1987. In both years, nids throughout the season, in spite of an extremely oxygen concentrations gradually returned to near- low phytoplankton biomass. The most likely food saturation values in autumn. source for the daphnids during this time is detritus and attached bacteria, as has been shown in other studies (Kamjunke et al., 1999; Picard & Lair, 2000). Discussion The low oxygen concentrations that were measured in The long-term data set from Lake Zwemlust presen- the summers following both biomanipulations (Fig. 5) ted here does not allow us to separate unambiguously indicate that during this phase primary production the two ‘alternative stable states’ that minimal models was low relative to heterotrophic activity. The ‘trans- predict for shallow lakes (Scheffer, 1990; Scheffer ition state’ provides suitable light and nutrient con- et al., 1993; Hosper, 1998). Some years can be clearly ditions for macrophytes to establish. However, characterised as either turbid and phytoplankton- observations in Lake Zwemlust in the last year of dominated (i.e. 1986, 1997, 1998) or as clear and this study indicate that these conditions may initially macrophyte-dominated (i.e. 1989–91). For many other favour filamentous algae and the establishment of years, however, it is not possible to place them into macrophytes may be delayed. one of these two categories, because they show Once macrophytes have reached a high biomass, characteristics of both. the lake enters the clear state (C in Fig. 6). This state Figure 6 summarises the developments in Lake can last for several years. It is characterised by a Zwemlust, within the conceptual framework of relatively high macrophyte abundance during the ‘alternative stable states’. Four different ‘states’ are whole summer, low algal densities, and high water

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2380–2387 2386 W.J. Van De Bund and E. Van Donk transparency. The situation in this period is not stable The success of fish stock reduction to restore clear- in the long term, however; probably under the water conditions in Lake Zwemlust with its continu- influence of grazing by birds and fish, species shifts ously high nutrient inputs demonstrates the potential in the macrophyte community were observed, from of this measure as a short-term management strategy. Elodea nuttallii to Ceratophyllum demersum to Potamog- Our data also indicate, however, that the clear state in eton berchtoldii (Van Donk & Otte, 1996; Van Donk, this lake with a dominance of macrophytes is not 1998). With the appearance of the latter species, a stable in the long term. As long as nutrient levels are ‘clear ⁄turbid’ phase (D in Fig. 6) starts, where periods high, there is a risk that macrophytes will not of clear water and algal blooms occur within the same successfully establish in a certain year, and if year. One of the factors likely to favour these blooms macrophytes miss their ‘window of opportunity’ to is the strong decline of P. berchtoldii in late summer proliferate on the lake bottom, phytoplankton may when the plant starts to form overwintering structures take over again, resulting in a return to the turbid (Van Donk, 1998). Furthermore, P. berchtoldii is much state. Consequently, reduction of nutrient loading to a more susceptible to periphyton cover than the other level where the clear, macrophyte-dominated situ- macrophyte species occurring in Lake Zwemlust; ation is stable is necessary to keep Lake Zwemlust progressive cover with periphyton is considered an clear in the long term. As long as the ultimate goal of important cause of the decline of P. berchtoldii (Van reducing nutrient loads is not achieved, repeated fish Donk & Gulati, 1995). With increasing frequency and stock reduction is a reasonable short-term manage- intensity of algal blooms, the lake gradually shifts to ment strategy. the ‘turbid’ state (A), the only state that appears to be genuinely stable in Lake Zwemlust. Acknowledgments Ultimately the decline in water quality from the macrophyte-dominated state to the turbid state is This study was financially supported by the EU- driven by continuously high nutrient inputs (Timms Environment project SWALE. We would like to & Moss, 1984; Scheffer et al., 1993). The long-term data thank S. van Rouveroy van Nieuwaal for compiling presented in this paper do not allow us to identify a the data set, and Klaas Sieuwertsen for assistance in single factor that causes the return to the turbid the field. situation, but rather several contributing factors can be recognised. The single most important factor References appears to be the succession in the macrophyte community towards a dominance of Potamogeton Barko J.W. & James W.F. (1998) Effects of submerged berchtoldii. Grazing on macrophytes by birds and fish aquatic macrophytes on nutrient dynamics, sedimen- apparently contributed to this succession of macro- tation, and resuspension. In: The Structuring Role phyte species in the lake (Van Donk & Otte, 1996; Van of Submersed Macrophytes in Lakes (Eds E. Jeppesen, Donk, 1998). In addition to changes in the macrophyte M. Søndergaard, M. Søndergaard & K. Christoffersen), pp. 197–217. Springer, Berlin. community, a shift in the size structure of zooplank- Benndorf J. (1995) Possibilities and limits for controlling ton towards smaller taxa (Fig. 2), with a correspond- eutrophication by biomanipulation. Internationale Revue ing decrease in grazing potential, appears to be der Gesamten Hydrobiologie, 80, 519–534. another important factor fostering the return of Hansson L.A., Annadotter H., Bergman E., Hamrin S.F., phytoplankton blooms. The cause of the decline of Jeppesen E., Kairesalo T., Luokkanen E., Nilsson P.A., large daphnids does not become clear from the Søndergaard M. & Strand J. (1998) Biomanipulation as available data. However, feeding of planktivorous an application of food-chain theory: constraints, fish is not the main reason, because large daphnids synthesis, and recommendations for temperate lakes. were present until 1994, although rudd had reached a Ecosystems, 1, 558–574. high biomass already in 1990 (Fig. 4). The refuge Hosper S.H. (1998) Stable states, buffers and switches: an offered by the macrophytes probably protected the ecosystem approach to the restoration and manage- Water Science daphnids from effective fish predation (Timms & ment of shallow lakes in the Netherlands. and Technology, 37, 151–164. Moss, 1984).

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