Zooplankton, Phytoplankton and the Microbial Food Web in Two Turbid and Two Clearwater Shallow Lakes in Belgium

Zooplankton, phytoplankton and the microbial food web in two turbid and two clearwater shallow lakes in Belgium

Koenraad Muylaert1,*, Steven Declerck2, Vanessa Geenens1, Jeroen Van Wichelen1, Hanne Degans2, Jochen Vandekerkhove2, Katleen Van der Gucht1,4, Nele Vloemans1,4, Wouter Rommens3, Danny Rejas2,6, Roberto Urrutia1,7, Koen Sabbe1, Moniek Gillis4, Kris Decleer5, Luc De Meester2 and Wim Vyverman1 1Dept. Biology, University Gent, K.L. Ledeganckstraat 35, Gent, 9000, Belgium; 2Lab. Aquatic Ecology, KULeuven, Debériotstraat 32, Leuven, 3000, Belgium; 3Lab. Botany, KULeuven, Kasteelpark Arenberg 31, Heverlee, 3001, Belgium; 4Dept. Microbiology, University Gent, K.L. Ledeganckstraat 35, Gent, 9000, Belgium; 5Institute for Nature Conservation, Kliniekstraat 25, Brussel, 1070, Belgium; 6Current address: Laboratory of Limnology, Universidad Mayor de San Simón, Cochabamba, Bolivia; 7Centro EULA, Universidad de Concepcion, Concepcion, Chile; *Author for correspondence (e-mail: [email protected]; phone: +32 9 264 53 66; fax: +32 9 264 53 34)

Received 21 November 2001; accepted in revised form 19 November 2002

Key words: Alternative stable states, Biomanipulation, Eutrophic shallow lakes, Macrophytes, Phytoplankton, Zooplankton

Abstract

Components of the pelagic food web in four eutrophic shallow lakes in two wetland reserves in Belgium (‘Blan- kaart’ and ‘De Maten’) were monitored during the course of 1998–1999. In each wetland reserve, a clearwater and a turbid lake were sampled. The two lakes in each wetland reserve had similar nutrient loadings and occurred in close proximity of each other. In accordance with the alternative stable states theory, food web structure differed strongly between the clearwater and turbid lakes. Phytoplankton biomass was higher in the turbid than the clearwater lakes. Whereas chlorophytes dominated the phytoplankton in the turbid lakes, cryptophytes were the most important phytoplankton group in the clearwater lakes. The biomass of microheterotrophs (bacteria, heterotrophic nanoﬂagellates and ciliates) was higher in the turbid than the clearwater lakes. Biomass and community composition of micro- and macrozooplankton was not clearly related to water clarity. The ratio of macrozooplankton to phytoplankton biomass – an indicator of zooplankton grazing pressure on phytoplankton – was higher in the clearwater when compared to the turbid lakes. The factors potentially regulating water clarity, phytoplankton, microheterotrophs and macrozooplankton are discussed. Implications for the management of these lakes are discussed.

Abbreviations: CPUE – catch per unit effort, HNF – heterotrophic nanoﬂagellates, SPM – suspended particulate matter

Introduction are relatively clear with low phytoplankton biomass and dense stands of submerged macrophytes. Under Because of intensive exchange of nutrients between the influence of eutrophication, these clearwater lakes their water columns and sediments, shallow lakes are become more turbid. Phytoplankton blooms develop sensitive to eutrophication (e.g., Ekholm et al. and submerged macrophytes disappear due to a lack (1997)). When nutrient loading is low, shallow lakes of light. Due to the loss of submerged macrophyte 138 stands, this transition is usually associated with a loss carried out during 1998–2000 in the framework of the of structural diversity and, as a result, a decrease in Flemish Impulse Program for Nature Development biodiversity at the higher trophic levels takes place (VLINA). In four lakes from two important wetland (e.g., Hanson and Butler (1994) and Scheffer (1998)). reserves in Belgium, all components of the pelagic At the same time, the transition results in a loss of food web were monitored during two years. In con- important socio-economical functions like the recre- trast to many previous studies of shallow lakes, this ational use of the lake for swimming or its use as a study also included microheterotrophs like bacteria, source of drinking water. While oligotrophic lakes are heterotrophic nanoflagellates and ciliates, important generally clear and hypertrophic lakes frequently tur- components of the microbial food web. Here we bid, shallow lakes at intermediate nutrient concentra- present an initial account and general overview of the tions may exhibit either clearwater or turbid states results and aim at evaluating the potential factors reg- (Scheffer et al. 1993). Many, predominantly biologi- ulating water clarity in these lakes. Based on these cal, feedback mechanisms stabilise these alternative conclusions, some recommendations for the develop- states. As a consequence, during eutrophication, the ment of management strategies aimed at restoring the clearwater state is often maintained until nutrients clearwater state in the lakes were formulated. reach high levels. Conversely, turbid shallow lakes often do not respond to even major nutrient reductions and remain turbid. The stability of each state Materials and methods depends on the nutrient levels: at increasing nutrient levels, there is a decrease in the stability of the clear- Study sites water state and an increase in the stability of the turbid state. Several studies have demonstrated that it is Four shallow lakes from two nature reserves were se- possible to reconvert turbid shallow lakes to clearwa- lected for this study (Figure 1). Both reserves are im- ter lakes (e.g., Meijer et al. (1999)) when reductions portant wetlands in Belgium and are protected by na- in nutrient loading are accompanied by the applica- tional and international agreements. Two lakes, lake tion of management strategies that alter the structure Visvijver and lake Blankaart, are situated in the of the food web itself (biomanipulation, Shapiro and ‘Blankaart’ wetland reserve (Diksmuide, Province of Wright (1984)). West-Vlaanderen), in the South-West of Belgium, Like many low-lying countries in Western Europe, close to the coast. It is positioned close the river Ijzer Belgium has numerous wetlands. Due to the advent and is frequently flooded by this river in winter, re- of industrial activity as well as an intensification of sulting in the two lakes being connected. The lakes agriculture, many of these wetlands have received were created by peat digging and are on average high nutrient inputs during the previous century and about 1 m deep. Lake Blankaart is the larger of the as a result many are severely eutrophied. Shallow two (surface area 32 ha) and receives surface water lakes are the dominant lake type in Flanders and, loaded with nutrients and sediments via two rivulets. where many of these lakes were of the clearwater type Nutrient inputs through these rivulets are very high and possessed rich submerged vegetations in the past, due to intensive agriculture and stock breeding in the most are now eutrophic and turbid (e.g., Denys catchment. Lake Visvijver is a small lake (0.6 ha) re- (1997)). These shallow lakes have a potentially high ceiving no surface water inputs. Both lakes were ecological value if submerged vegetations are re- dredged in 1995 to remove sediment and associated stored. This can be attained by applying appropriate nutrients. Simultaneously, the fish community was management strategies. However, to develop effective manipulated in lake Visvijver, but not in lake Blan- management strategies, a good knowledge of the kaart. These management activities resulted in the functioning of the ecosystem is required. In contrast transition to a clearwater state in lake Visvijver but to many other Western European countries, relatively had no effect on lake Blankaart (Peeters et al. 1996). few studies have been carried out in Belgium with The two other lakes, lake Maten 12 and lake Maten respect to the functioning of shallow lakes. To 13, are situated in the ‘De Maten’ wetland reserve in achieve a better knowledge on shallow lakes in Bel- the North-Eastern part of Belgium (Genk, Province of gium and to provide a framework for developing Limburg). The ‘De Maten’ reserve contains a total of management strategies aimed at restoring the clear- 32 small lakes with a surface area ranging from 0.5–9 water state in shallow lakes, a research study was ha (lake Maten 12: 3.2 ha, lake Maten 13: 3.3 ha). 139

Figure 1. The location of the ‘Blankaart’ (B) and ‘De Maten’ (M) wetland reserves in Belgium (left) and detailed maps at identical scales of the four lakes studied (right). Scale bar is 500 m.

The ‘De Maten’ lakes were created by peat digging Bacteria were stained with DAPI, filtered onto 0.2 around the year 1400 and have been used for fish cul- ␮m pore size membrane filters and counted using epi- ture until 1991. All lakes in this pond system are di- fluorescence microscopy (Porter and Feig 1980). rectly or indirectly connected by a system of over- Counts were converted to biomass assuming a cellu- flows and are fed by surface water via two main lar carbon content of 2 10−11 mg C cell−1 (Lee and rivulets (Cottenie et al. 2001). Between the two ‘De Fuhrman 1987). HNF were also stained with DAPI, Maten’ lakes studied, water flows from lake Maten 13 filtered onto 0.8 ␮m pore size membrane filters and to lake Maten 12. enumerated using epifluorescence microscopy (Sherr et al. 1993). Three size classes were discerned during Sampling and analyses enumeration (< 4 ␮m, 4–10 ␮mand>10␮m). Cili- ates were enumerated using inverted microscopy af- All lakes were sampled monthly during winter and ter staining with Bengal rose to facilitate the distinc- biweekly during summer from January 1998 to De- tion between living organisms and detritus. Ciliates cember 1999, resulting in 34 sampling occasions in were identified up to genus level where possible or each lake. Subsurface samples were collected during were assigned to a given size class (< 20 ␮m, 20–40 daytime at a fixed sampling station in each lake. Tem- ␮mor>40␮m). For conversion of HNF and ciliate perature, pH and Secchi depth were measured at the abundances to biomass, in each lake and for all gen- time of sample collection. Samples for bacteria, het- era or size classes, 25–100 individuals from different erotrophic nanoflagellates (HNF), ciliates and phy- samples were measured. For each lake, an annual av- toplankton were fixed in the field using Lugol’s solu- erage biovolume was calculated for each genus or tion, formalin and thiosulphate (Sherr et al. 1989). size class. Biovolume was converted to biomass us- Macrozooplankton was sampled using a Schindler- ing a conversion factor of 15 10−11 mg C ␮m−3 for Patalas trap. The trap was deployed at different depths HNF (Fenchel 1982) and 22 10−11 mg C ␮m−3 for to include the entire water column. Macrozooplank- ciliates (Putt and Stoecker 1989). Phytoplankton was ton samples were fixed with sucrose-saturated forma- identified up to genus level and enumerated using in- lin (Haney and Hall 1973). Rotifers were collected verted microscopy. For each lake, of each genus, quantitatively by filtering 0.5–3 l water through a 30 25–50 cells from different samples were measured. ␮m pore size nylon mesh. The mesh containing the For each lake, an average biovolume was calculated rotifers was stored in 30 ␮m filtered lake water fixed for each genus and biovolume was converted to bio- with 5% w/v formalin. A whole water sample was mass using the formulations given by Menden-Deuer transferred to the laboratory (cooled and darkened) to and Lessard (2000). Macrozooplankton was enumer- be subsampled for dissolved nutrients and suspended ated using a dissection microscope. Cladocerans were particulate matter (SPM). identified up to species level while copepods were 140 identified to the order level. For each taxon in each to reduce skewness and approximate normal distribu- sample, 30 individuals were measured to convert tion. abundances to biomass using published length-weight regressions (Bottrell et al. 1976). For quantification of rotifers, the organisms were washed off the nylon Results mesh and enumerated using a dissection microscope. All individuals were identified to species level where Concentrations of dissolved inorganic nitrogen (the possible or to genus level. Abundances were con- sum of nitrate, nitrite and ammonium) were higher in verted to biomass using published data on biomass the lakes of the ‘Blankaart’ wetland reserve than the content of the taxa encountered (Ruttner-Kolisko ‘De Maten’ reserve (Table 1, Figure 2). Of the two 1974; Dumont et al. 1975; Pontin 1978). Samples for lakes of the ‘Blankaart’ reserve, dissolved inorganic dissolved nutrients were filtered over a GF/F filter and nitrogen concentrations were highest in lake Blan- stored frozen until analysed using a Skalar autoanaly- kaart, where concentrations up to 20 mg N l−1 were ser according to the methods described in Greenberg measured. Dissolved inorganic nitrogen concentra- et al. (1992). No data on total phosphorus or nitrogen tions were nearly an order of magnitude lower in the are available. Suspended particulate matter (SPM) lakes of the ‘De Maten’ wetland reserve and were concentrations were determined gravimetrically after lowest in lake Maten 13. In the ‘Blankaart’ lakes, and filtration of a known volume of water onto a pre- to a lesser extent in the ‘De Maten’ lakes, nitrogen weighed GF/F filter. concentrations decreased over summer (Figure 3). Twice each year (May and August), the percent- Dissolved phosphorus concentrations were also max- age cover by submerged macrophytes was determined imal in the ‘Blankaart’ lakes, with lake Visvijver hav- along several transects in the lakes and extrapolated ing the highest phosphorus levels (Table 1, Figure 2). to the entire lake surface. Fish biomass and commu- Dissolved phosphorus concentrations were close to an nity composition were estimated once in September order of magnitude lower in the lakes of the ‘De 2000 using multi-mesh size gill nets (Jeppesen et al. Maten’ reserve. Of the two ‘De Maten’ lakes, Maten 1999). We used 42 m long, 0.75–1.5 m wide nets 13 had the lowest phosphorus levels, with concentra- subdivided in equal sections of 3 m length with mesh tions approaching detection limit on several occasions sizes ranging from 6.25 to 70 mm. Nets were placed during the study. In contrast to nitrogen, phosphorus in the littoral as well as the open water around sunset did not display a clear seasonal trend in the lakes and were sampled about 16 h later. Four nets were (Figure 3). pH was generally more than one unit placed in lake Blankaart and the ‘De Maten’ lakes higher in the ‘Blankaart’ lakes than the ‘De Maten’ while only two nets were used in the smaller lake lakes (Table 1). Visvijver. Ten individuals of each species were SPM concentrations and Secchi depth were mea- weighed and measured and catches were converted to sured as indicators of water clarity (Table 1, Figures ‘catch per unit effort’ (CPUE), which is the total wet 2 and 4). In both wetland reserves, the two lakes stud- biomass per net. ied differed strongly with respect to water clarity. SPM concentrations were highest and Secchi depth Statistical analyses lowest in lake Blankaart and lake Maten 12. Lake Visvijver and lake Maten 13 had lowest SPM concen- We compared biomass and biomass ratios of different trations and the lake bottom was, apart from a single components of the food web between the two lakes sampling occasion, always visible. In each wetland in each wetland reserve using t-tests. As in each wet- reserve, the difference in SPM concentrations be- land reserve, the two lakes studied are interconnected tween the two lakes was highly significant (t-test: at least during part of the year and have comparable ‘Blankaart’ as well as ‘De Maten’ p < 0.0001). Given nutrient levels, our null hypothesis was that biomass these strong differences in water clarity among the or biomass ratios of components of the food web are lakes studied, we will refer to lake Blankaart and lake similar in the two lakes of each wetland reserve. As Maten 12 as the turbid lakes and lake Visvijver and within-lake seasonal variation often exceeded be- lake Maten 13 as the clearwater lakes. tween-lake differences, paired t-tests were used in Submerged macrophyte vegetations were only ob- which data from the same sampling dates were com- served in the clearwater lakes (Table 1, Figure 2). pared. All data were log-transformed before analysis During this survey, percentage cover by submerged 141

Table 1. Averages for some important variables measured in the four lakes studied (1998 and 1999). Dissolved nitrogen is the sum of nitrate, nitrite and ammonia. For phytoplankton, ciliates, micro- and macrozooplankton and ﬁsh, the average percentage contribution of some important taxonomical/functional groups to annual average total biomass is given next to the average biomass of these groups.

‘Blankaart’‘De Maten’ Variable Blankaart Visvijver Maten 12 Maten 13

Abiotic variables pH 8.5 8.5 7.2 7.1 SPM (mg l−1) 43 6 19 9 Secchi depth (m) 0.37 lake bottom 0.36 lake bottom Nutrients dissolved phosphorus (␮gl−1) 280 460 45 18 dissolved nitrogen (␮gl−1) 5880 750 207 99 Phytoplankton (␮gCl−1) 1190 160 430 180 Chlorophyta 757 (46%) 21 (10%) 125 (30%) 69 (23%) Cryptophyta 137 (17%) 94 (63%) 41 (14%) 55 (35%) Euglenophyta 71 (6%) 1 (< 1%) 148 (24%) 20 (9%) Incertae Sedis 38 (5%) 31 (16%) 41 (16%) 11 (15%) Cyanobacteria 86 (8%) 9 (5%) 32 (5%) 2 (1%) Bacillariophyta 95 (17%) 3 (4%) 16 (5%) 4 (3%) Dinophyta 5 (< 1%) 2 (< 1%) 10 (3%) 16 (10%) Chrysophyta 2 (< 1%) 1 (< 1%) 6 (2%) 4 (4%) Xanthophyta 1 (< 1%) 0 (< 1%) 11 (2%) 1 (< 1%) Microheterotrophs (␮gCl−1) Bacteria 262 134 170 130 HNF 22 2.4 9 3.4 Ciliates 177 47 233 53 oligotrich ciliates 124 (68%) 24 (73%) 57 (40%) 29 (57%) other ciliates 53 (32%) 23 (27%) 176 (60%) 24 (43%) Microzooplankton (␮gCl−1) 916 517 338 255 Asplanchna 75 (4%) 7 (2%) 26 (8%) 8 (4%) other rotifers 349 (41%) 289 (49%) 187 (56%) 122 (42%) copepod nauplii 492 (55%) 221 (49%) 125 (36%) 125 (53%) Macrozooplankton (␮gCl−1) 1478 524 344 240 cyclopoid copepods 850 (62%) 316 (53%) 131 (29%) 37 (22%) calanoid copepods 0 (0%) 18 (9%) 26 (11%) 68 (30%) Bosmina 454 (19%) 35 (9%) 150 (45%) 32 (21%) Daphnia 172 (13%) 28 (17%) 21 (9%) 90 (11%) Ceriodaphnia 0 (0%) 122 (9%) 8 (2%) 6 (3%) Submerged macrophytes (% cover) 055043 Fish (CPUE in g net−1) 1714 0 420 202 Planktivorous fish 566 (33%) 0 259 (62%) 192 (95%) Benthivorous fish 1129 (66%) 0 0 (0%) 10 (5%) Piscivorous fish 20 (1%) 0 161 (38%) 0 (0%) macrophytes was around 50% in both clearwater lucens dominated the submerged vegetation, with lakes. In lake Visvijver, the dominant macrophyte was Utricularia vulgaris also being commonly observed. Chara globularis, while floating beds of filamentous Phytoplankton biomass was significantly higher in algae covered a large part of the lake surface towards the turbid than in the clearwater lakes (t-test: ‘Blan- the end of summer. In lake Maten 13, Drepanocladus kaart’ as well as ‘De Maten’ p < 0.0001), with lake fluitans, Polygonum amphibium and Nitella trans- Blankaart having highest biomass (Table 1, Figure 4). The phytoplankton community in the turbid lakes was 142

Figure 2. a–d: Median values (horizontal line) and 25 (top of box) and 75 percentiles (bottom of box) for some important chemical and physical variables. e: Fish biomass (as catch per unit effort or CPUE) and community composition as measured in September 2000. f: The average (May and August in 1998 and 1999) cover by submerged macrophytes. dominated by chlorophytes (mostly coenobial taxa 5). Differences in heterotrophic protistan biomass be- like Scenedesmus) while, in the clearwater lakes, tween turbid and clearwater lakes were more pro- cryptophytes were the dominant group of algae. High- nounced than differences in bacterial biomass (Table est biomass of cyanobacteria was observed in lake 1, Figure 4). Biomass of ciliates was much higher Blankaart, where a Planktothrix bloom developed to- than that of HNF in all lakes. Combined biomass of wards the end of the summer in 1998. In the turbid heterotrophic protists (HNF and ciliates), as well as lakes, phytoplankton biomass increased gradually biomass of HNF and ciliates separately, was on aver- over summer (Figure 3). In the clearwater lakes, age higher in the turbid than in the clearwater lakes. blooms developed rather irregularly between spring This difference was signiﬁcant for ciliates as well as and autumn. During summer, phytoplankton biomass HNF (t-test: ‘Blankaart’ and ‘De Maten’ p < 0.0001, tended to be low in the clearwater lakes. both for ciliates and HNF). Oligotrich ciliates were Bacterial biomass was, like phytoplankton bio- relatively more important in the lakes of the ‘Blan- mass, signiﬁcantly higher in the turbid than in the kaart’ reserve than in those from the ‘De Maten’ re- clearwater lakes (t-test: ‘Blankaart’ p < 0.0002 and serve. ‘De Maten’ p < 0.01), with maximal average biomass In contrast to phytoplankton, bacteria and het- occurring in lake Blankaart (Table 1, Figure 4, Figure erotrophic protists, biomass of micro- as well as mac- 143

Figure 3. Temporal dynamics of suspended particulate matter (SPM) concentration, dissolved phosphorus concentration, dissolved inorganic nitrogen concentration (nitrate + nitrite + ammonia) and phytoplankton biomass in the lakes from the ‘Blankaart’ (left) and the ‘De Maten’ (right) wetland reserves in 1998 and 1999. Note different scales for the ‘The Blankaart’ lakes and the ‘De Maten’ lakes. rozooplankton seemed not to be clearly related to wa- mass of microzooplankton also was significantly ter clarity (Table 1, Figure 4). Biomass of higher in the turbid lake in the ‘Blankaart’ reserve (t- macrozooplankton was significantly higher in the tur- test: p < 0.05) but did not differ significantly between bid lake in the ‘Blankaart’ reserve (t-test: p < 0.01) the two lakes from the ‘De Maten’ reserve (t-test: p = but did not differ significantly between the two lakes 0.46). In the clearwater lakes, total zooplankton bio- from the ‘De Maten’ reserve (t-test: p = 0.059). Bio- mass was generally highest during spring. In the tur- 144

Figure 4. a–c, e, g, i: Median values (horizontal line) and 25 (top of box) and 75 percentiles (bottom of box) for some important biological variables. d, f, h, j: Percentage contribution of some important groups to total biomass of phytoplankton (d), ciliates (f), microzooplankton (h) and macrozooplankton (j). 145 bid lakes, total zooplankton biomass peaked during Discussion summer (Figure 5). Of all lakes, the biomass of macrozooplankton was on average highest in lake Blan- Dissolved inorganic nutrient concentrations in the kaart. Biomass of microzooplankton was comparable lakes from the ‘Blankaart’ wetland reserve exceeded to macrozooplankton biomass in all lakes except lake those from the lakes in the ‘De Maten’ reserve by Blankaart, where macrozooplankton biomass was nearly an order of magnitude. In both wetland re- about twice as high as microzooplankton biomass. serves, dissolved nutrient concentrations in the two Copepod nauplii and rotifers contributed equally to lakes studied were comparable. This is not surprising, total microzooplankton biomass in all lakes. The car- given the fact that the lakes in both reserves were at nivorous rotifer Asplanchna contributed on average least during some part of the year interconnected. only 2–8% of total microzooplankton biomass in the Flooding of the small dike separating the clearwater lakes studied. The percentage contribution of daph- lake Visvijver from the turbid lake Blankaart occurs nids (Daphnia and Ceriodaphnia) to total macrozo- regularly in winter, resulting in an exchange of water oplankton biomass was slightly higher in the clearwa- between both lakes. Lake Maten 13 discharges into ter lakes than in the turbid lakes, but this difference lake Maten 12 by an overflow system and both lakes was only significant in the ‘Blankaart’ reserve (t-test: are fed by the same rivulet. Despite the fact that the ‘Blankaart’ p < 0.05 and ‘De Maten’ p = 0.88). two lakes in both wetland reserves had similar nutri- To estimate the grazing impact of macrozooplank- ent concentrations, a clearwater and a turbid lake ton on phytoplankton, the macrozooplankton to phy- were present in each wetland reserve. This observa- toplankton biomass ratio was calculated as an indica- tion supports the alternative stable states theory tor of macrozooplankton grazing pressure on (Scheffer et al. 1993) in that water clarity may differ phytoplankton (Table 2). In each wetland reserve, the strongly in shallow lakes having similar water chem- biomass ratio of total macrozooplankton (t-test: istry. The fact that a clear and a turbid lake occurred ‘Blankaart’ p < 0.001 and ‘De Maten’ p < 0.005) or in both wetland reserves despite large differences in daphnids (t-test: ‘Blankaart’ p < 0.0005 and ‘De nutrient concentrations between the two reserves il- Maten’ p < 0.05) over phytoplankton was signifi- lustrates that alternative stable states may occur over cantly higher in the turbid when compared to the a wide range of nutrient loadings. In general, it is as- clearwater lake. While the macrozooplankton to phy- sumed that at total phosphorus concentrations exceed- toplankton ratio differed only about 5-fold between ing 100–150 ␮gl−1, a stable clearwater state cannot the clearwater and turbid lakes, the daphnids to phy- be achieved (Jeppesen et al. 1990; Hosper and Jagt- toplankton ratio was 16 and 24 times higher in the man 1990). Although unfortunately no data on total clearwater than the turbid lake in the ‘Blankaart’ and phosphorus were available for this study, with an av- ‘De Maten’ reserve, respectively. erage dissolved phosphorus concentration of 460 Fish biomass (as CPUE) tended to be higher in the ␮gl−1, this limit must have been exceeded in lake turbid than the clearwater lakes, with lake Blankaart Visvijver. having highest fish biomass (Table 1, Figure 2). No Water clarity in the four lakes studied was related fish were caught in lake Visvijver, where a period of to food web structure rather than nutrient concentra- anoxia preceded a massive fish kill in 1998. Plank- tion. Biomass of phytoplankton and microheterotro- tivorous and benthivorous species like white bream phs, the zooplankton to phytoplankton ratio, occur- (Blicca bjoerkna), roach (Rutilus rutilus) and bream rence of submerged macrophytes and the fish (Abramis brama) dominated in lake Blankaart while community differed markedly between the clearwater the exotic and piscivorous brown bullhead (Ameiurus and turbid lakes. Phytoplankton biomass was nearly nebulosus) and (to a lesser extent) roach and rudd twice as high in the turbid lakes when compared to (Scardinius erythrophtalmus) were the most impor- the clearwater lakes. Being a component of the tant species observed in lake Maten 12. In lake Maten seston, phytoplankton contributes to total SPM and 13 rudd and tench (Tinca tinca) dominated the fish may therefore be a direct cause of high suspended community with the exotic pumpkinseed (Lepomis matter concentrations in turbid lakes. When phy- gibbosus) and topmouth gudgeon (Pseudorasbora toplankton biomass was converted to dry weight (as- parva) being common too. suming a carbon to dry weight ratio of 0.5, Reynolds (1984)), however, phytoplankton accounted only for on average 5.9% (maximum 22%, in lake Blankaart) 146

Figure 5. Temporal dynamics of bacterial biomass, biomass of heterotrophic protists (HNF + ciliates), biomass of microzooplankton (rotifers + copepod nauplii) and macrozooplankton biomass in the lakes from the ‘Blankaart’ (left) and the ‘De Maten’ (right) wetland reserves in 1998 and 1999. Note different scales for the ‘Blankaart’ lakes and the ‘De Maten’ lakes. or 5.1% (maximum 14%, in lake Maten 13) of total sediment levels in the turbid lakes. Submerged mac- suspended matter in the turbid lakes. Therefore, al- rophytes covered about half the lake surface in the though high SPM concentrations are associated with clearwater lakes but were absent in the turbid lakes. high phytoplankton biomass, phytoplankton cannot When forming a dense vegetation, submerged macro- be the only factor responsible for the high suspended phytes may reduce water column turbulence and in- 147

Table 2. Average ratios of zooplankton biomass over phytoplankton biomass in the four lakes studied.

‘Blankaart’‘De Maten’ Ratio Blankaart Visvijver Maten 12 Maten 13

Macrozooplankton/phytoplankton 1.6 6.7 0.9 4.4 Daphnids/phytoplankton 0.15 2.4 0.09 2.1 crease water clarity through a reduction of sediment mass nor community composition, however, is a good resuspension and an increase in SPM sedimentation indicator of zooplankton grazing pressure on phy- rates (e.g., James and Barko (1990) and Jones toplankton. We calculated the ratio of zooplankton (1990)). In turbid lakes, no submerged macrophytes biomass over phytoplankton biomass as an indicator are present to reduce turbulence in the water column of zooplankton grazing pressure on phytoplankton. and, as a result, even low wind velocities may create This ratio was significantly higher in the clearwater turbulence that is strong enough to cause resuspen- than in the turbid lakes. Most zooplankton groups, sion of bottom sediments (Kristensen et al. 1992). like rotifers, copepods or Bosmina, graze selectively Differences in the fish community may also explain on specific phytoplankton size classes and are there- the difference in water clarity between the clear and fore generally considered incapable of efficiently con- turbid lakes. Benthivorous fish species attained high trolling phytoplankton biomass (Hansson and Car- biomass in the turbid lakes. Moreover, the piscivorous penter 1993; Havens 1993; Cyr and Curtis 1999). brown bullhead, which attained high biomass in the Only daphnids like Daphnia and Ceriodaphnia have turbid lake Maten 12, also has a benthic lifestyle. high clearance rates on a wide size-range of particles Through their foraging activities, fish communities and capable of regulating phytoplankton biomass from the turbid lakes may contribute substantially to (Hall et al. 1976). The biomass ratio of daphnids to sediment resuspension (cf. Meijer et al. (1990) and phytoplankton was also significantly higher in the Havens (1991)). Next to the presence of macrophyte clearwater when compared to the turbid lakes. More- stands, which prevent resuspension and promote sed- over, the difference between clearwater and turbid imentation of suspended matter, low biomass or com- lakes with respect to this ratio was much higher for plete absence of benthivorous fish may be an addi- daphnids than for total macrozooplankton. This sug- tional cause of the low SPM concentrations in the gests than grazing by daphnids may play an impor- clearwater lakes. tant role in regulating phytoplankton biomass in the Total nutrient concentrations were similar in the clearwater lakes. clear and turbid lakes in both wetland reserves stud- Like for phytoplankton biomass, microhet- ied, while phytoplankton biomass differed about two- erotrophic components of the microbial food web fold. Therefore, some factor other than nutrients must (bacteria, HNF and ciliates) attained significantly have been regulating phytoplankton biomass in the higher biomass in the turbid than in the clearwater clearwater lakes. In shallow lakes, macrozooplankton lakes. To a large extent, these microheterotrophs de- are generally considered to be the dominant grazers pend directly or indirectly on phytoplankton as a food on phytoplankton. Macrozooplankton is in turn source. Exudates produced by phytoplankton are an preyed upon by planktivorous fish. Planktivorous fish important substrate for aquatic bacteria in shallow influence macrozooplankton biomass as well as com- lakes (Kamjunke et al. 1997). HNF and ciliates feed munity composition, as certain macrozooplankton on bacteria (e.g., Sanders et al. (1989)) and small groups like Bosmina and copepods are able to avoid phytoplankton (e.g., Weisse et al. (1990)). The low fish predation (Verity and Smetacek 1996; Slusarczyk biomass of bacteria, HNF and ciliates in the clearwa- 1997) while the relatively large daphnids are highly ter lakes may therefore reflect lower food availability. sensitive to fish predation (e.g., Brooks and Dodson Top-down regulation, however, may also explain the (1965) and Schriver et al. (1995)). In the four lakes lower biomass of the components of the microbial studied, however, no clear relation could be found food web in the clearwater lakes. Daphnids are non- between CPUE of planktivorous fish and total mac- selective filter feeders whose filter apparatus is capa- rozooplankton biomass or the contribution of daph- ble of retaining particles down to about 1 ␮m in size nids to macrozooplankton biomass. Neither total bio- (Brendelberger 1991). Phytoplankton, bacteria, HNF 148 and ciliates comprise potential food items for daph- between the ponds in de Maten reserve probably also nids (Jürgens 1994). Therefore, if grazing by daph- results from differences in water level regime. In con- nids affects phytoplankton populations, it is also trast to lake Maten 12, water levels in lake Maten 13 likely to affect bacterial, HNF and ciliate populations. are highly variable and often quite low. The pond In both wetland reserves, a clearwater and a turbid water level has repeatedly fallen dry during the last lake occurred next to each other in an interconnected decades. By impacting the fish community, such system and with virtually identical nutrient loading. events may have acted in a similar way as biomanip- This indicates that, in both wetland reserves, restora- ulation. In addition, low water levels may have stim- tion of the turbid lakes to the clearwater state should ulated the germination of submerged vegetations. be possible. The differences between the turbid and Both the successful biomanipulation of lakes in the the clearwater lakes are well in agreement with the Blankaart system and the impact of water levels on theory of the alternative stable states (Scheffer et al. food web structure in lake Maten 13 suggest that fish 1993) and suggest that the restoration of the clearwa- removal or temporal drainage may be a very promis- ter state in the turbid lakes can be accomplished by ing techniques for the restoration of the clearwater changes in food web structure rather than by water state in the turbid lakes of the two wetland reserves. quality improvement alone (Perrow et al. 1997; Hans- This is certainly true for lake Maten 12, as this lake son et al. 1998; Meijer et al. 1999). Such changes in is very similar to lake Maten 13 with respect to mor- food web structure can be achieved by the applica- phometry, size and water quality. In Lake Blankaart, tion of biomanipulation (Shapiro and Wright 1984; several small scale in situ enclosure experiments have Gulati et al. 1990). In practice, this method most of- resulted in strong increases in water clarity when fish ten involves a strong reduction of the planktivorous were excluded (Declerck et al. 1997; Declerck 2001). and benthivorous fish biomass via large scale fish re- In these experiments, a rapid growth of populations movals, often combined with stocking of piscivorous of large cladocerans was observed, resulting in strong fish (e.g., pike). The removal of planktivorous fish is reductions in phytoplankton biomass due to grazing. meant to allow for populations of large-bodied filter Such results indicate that planktivorous fish suppress feeding Cladocera to develop and gain control over large zooplankton in lake Blankaart and that bioma- phytoplankton by grazing. The reduction of the bio- nipulation may contribute to the restoration of the mass of benthic fish results in a decrease of sediment Blankaart system. However, a large proportion of the resuspension and associated nutrient release from the increase of water transparency may also have resulted lake sediments. A decrease in phytoplankton biomass from an enclosure artefact causing sedimentation of and the amount of suspended matter results in an in- algae and suspended matter. Moreover, a large scale crease in water clarity, resulting in opportunities for food web manipulation experiment that was carried the establishment of macrophytes. These macrophytes outina1hapart of the lake that was separated by a are now considered to stabilize the clearwater state net and in which a 60% removal of the benthic and through several positive feedback mechanisms (e.g., planktivorous fish biomass was combined with the Hansson et al. (1998)). introduction of pike fingerlings, did not result in any The difference in water clarity between the stud- increase of water transparency (Declerck et al. 2001). ied ponds is to a large extent due to differences in Extrapolation of the results of the successful food food web structure. Biomanipulation, for instance, web manipulations done in lake Visvijver should has been successfully applied in ponds of the Blan- therefore be made with care, as lake Blankaart differs kaart system. Although lake Visvijver originally was from lake Visvijver in many aspects. Lake Blankaart a turbid pond lacking submerged vegetation, the lake is considerably larger than lake Visvijver and is more switched to the clearwater state after it was dredged exposed to wind. Wind can be a very important cause in 1995 and biomanipulated during three subsequent of sediment resuspension in shallow lakes (Douglas years (Declerck et al. 2000; Declerck 2001). A simi- and Rippey 2000) and wind-induced waves can ham- lar result was obtained in lake Kasteelvijver, another per the development of submerged vegetation (Hos- lake in the Blankaart reserve. Although a large pro- per 1997). Furthermore, in contrast to lake Visvijver, portion of superficial sediments of lake Maten 12 is lake Blankaart is a very open system that is connected made up by peat, which is a potentially important with several rivulets. These rivulets allow an easy source of organic matter and humic acids that can in- immigration of fish. Moreover, via the rivulets, there crease water turbidity, the difference in water clarity is a continuous inflow of water rich in nutrients, sus- 149 pended matter and pesticides. If a large scale bioma- Declerck S. 2001. An ecological and ecological-genetic study of nipulation of lake Blankaart would be undertaken, Daphnia in a shallow hypertrophic lake. PhD Dissertation, Uni- these factors would hamper the development of sub- versity Gent. Declerck S., De Meester L., De Smedt P., Rommens W., Vyverman merged vegetation and would continuously have a de- W., Geenens V. et al. 2000. Clear water and charophytes in a stabilising effect on the clearwater state, decreasing hypertrophic pond. Verhandlungen Internationale Vereinigung the probability of a successful restoration on a long für Theoretische und Angewandte Limnologie 27: 541. term. We therefore advocate that large-scale food web Declerck S., De Meester L., Geenens V., Vyverman W., Rommens manipulations in Lake Blankaart should be preceded W. and Decleer K. 2001. Experimenteel ecologisch onderzoek naar de herstelkansen van het aquatisch ecosysteem van de by a drastic reduction in nutrient loading of the up- Blankaart door hydrologische isolatie en voedselwebmanipu- stream rivulets in the Blankaart catchment area. This latie. Report IN/KD/98.002. 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