Freshwater Biology (2001) 46, 1397±1408
APPLIED ISSUES
Dynamics of submerged macrophyte populations in response to biomanipulation J O H N A . S T R A N D and S T E F A N E . B . W E I S N E R Limnology, Department of Ecology, Lund University, Ecology building, Lund, Sweden
SUMMARY 1. A 6-year study (1992±97) of changes in submerged vegetation after biomanipulation was carried out in the eutrophicated Lake FinjasjoÈn, Southern Sweden. Ten sites around the lake were revisited each year. At each site ®ve samples of above-ground biomass were taken at 10 cm water depth intervals. An investigation of the seed bank at the 10 sites, and a grazing experiment where birds and large ®sh were excluded was also conducted. 2. Between 1992 and 1996, in shallow areas (water depth < 3 m), vegetation cover increased from < 3 to 75% and above-ground biomass from < 1 to 100 g DW m±2. Mean outer water depth increased from 0.3 to 2.5 m. Elodea canadensis and Myriophyllum spicatum accounted for > 95% of the increase in biomass and plant cover. The following year (1997), however, cover and above-ground biomass decreased, mainly attributable to the total disappearance of E. canadensis. Secchi depth increased after biomanipulation until 1996, but decreased again in 1997. 3. Total and mean number of submerged species increased after biomanipulation, probably as a result of the improved light climate. However, after the initial increase in species number there was a decrease during the following years, possibly attributed to competition from the rapidly expanding E. canadensis and M. spicatum. The lack of increase in species number after the disappearance of E. canadensis in 1997 implies that other factors also affected species richness. 4. A viable seed bank was not necessary for a rapid recolonization of submerged macrophytes, nor did grazing by waterfowl or ®sh delay the re-colonization of submerged macrophytes. 5. Submerged macrophytes are capable of rapid recolonization if conditions improve, even in large lakes such as FinjasjoÈn (11 km2). Species that spread by fragments will increase rapidly and probably outcompete other species. 6. The results indicate that after the initial Secchi depth increase, probably caused by high zooplankton densities, submerged vegetation further improved the light climate. The decrease in macrophyte biomass in 1997 may have caused the observed increase in phosphorus and chlorophyll a, and the decrease in Secchi depth. We suggest that nutrient competition from periphyton, attached to the macrophytes, may be an important factor in limiting phytoplankton production, although other factors (e.g. zooplankton grazing) are also of importance, especially as triggers for the shift to a clear-water state. Keywords: Elodea, Myriophyllum, nutrient competition, periphyton, Secchi depth
Correspondence: J. A. Strand, The Rural Economy and Agricultural Society, Lilla BoÈslid, S-310 31 Eldsberga, Sweden. E-mail:
[email protected] Ó 2001 Blackwell Science Ltd
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Introduction Biomanipulation has often been used as a management tool for lake restoration during the last decades (Jeppesen et al., 1990; Hansson et al., 1998). In theory, the removal of a large fraction of zooplanktivorous ®sh leads to increased zooplankton biomass and a subsequent increase in grazing pressure on phytoplankton (Shapiro, Lakarra & Lynch, 1975). The ultimate goal of biomanipulation (clear water) is thus reached by altering the biomass of higher trophic levels. However, an underlying assumption is that the ecosystem will stabilize in the clear water state through positive feedback mechanisms (Scheffer et al., 1993). In shallow, eutrophic lakes the clear water state is largely stabilized by increased submerged macrophyte growth because of improved light availability (Scheffer, 1990; Blindow et al., 1993; Scheffer et al., 1993). Submerged vegetation has a positive in¯uence on water clarity through a number of mechanisms, e.g. nutrient competition, improved possibilities for zooplankton to avoid ®sh predation (resulting in increased zooplankton grazing on phytoplankton), allelopathy and decreased sediment resuspension (e.g. Timms & Moss, 1984; Moss, 1990; Scheffer, 1990; Blindow et al., 1993; Scheffer et al., 1993; Hargeby et al., 1994; Schriver et al., 1995; Bekliouglu & Moss, 1996). A large number of biomanipulation projects have failed or have been only partially successful (Hansson et al., 1998). Although phytoplankton biomass has often been substantially reduced during the season after biomanipulation, lakes often return to the turbid state only after a few years (Hansson et al., 1998). Positive, long-term effects of biomanipulation seem to depend to a large extent on the development of the submerged vegetation (van Dijk & van Donk, 1991; Hansson et al., 1998). It is, therefore, important to understand the factors determining the dispersal and establishment of submerged macrophytes when a lake shifts to the clear water state. For example, waterfowl grazing can have pronounced effects on submerged macrophytes in shallow eutrophic temperate lakes (Lauridsen, Jeppesen & éstergaard-Andersen, 1993; Lauridsen, Jeppesen & Sùndergaard, 1994; Sùndergaard et al., 1996; Weisner, Strand & Sandsten, 1997; Strand, 1999a), and might delay the re-colonization of submerged vegetation (Lauridsen et al., 1994). An existing seed bank is another factor that has been
postulated as important for the re-colonization of submerged macrophytes (Hosper & Meijer, 1992). Although the importance of re-colonization of submerged macrophytes has been emphasized, few studies have been carried out with the focus on clarifying the structuring forces for colonization of different submerged species after biomanipulation projects in large lakes (but see Strand, 1999b). Previous studies have mainly concerned relatively small lakes (< 1 km2) (Ozimek, Gulati & van Donk, 1990; Lauridsen et al., 1993; Hansson et al., 1998). In this paper, we present data from a 6-year monitoring project of the dynamics of submerged macrophyte populations before, during and after biomanipulation of a large (11 km2) eutrophicated lake. We also did seed bank and grazing experiments to elucidate factors affecting the development of macrophyte populations.
Methods Lake description (prior to biomanipulation) Prior to biomanipulation, FinjasjoÈn was a large, phytoplankton dominated lake (area 11.0 km2, mean depth 2.7 m, maximum depth 12 m) (Annadotter et al., 1999). It is a eutrophicated lake and the mean summer concentration of nutrients before biomanipulation was high and variable with a mean for total phosphorous of 0.23 mg L±1 and for total nitrogen of 1.4 mg L±1. Chlorophyll a varied between 50 and 120 lg L±1 and Secchi depth was about 0.3 m (Hansson et al., 1998). Cyprinids like roach (Rutilus rutilus L.) and bream (Abramis brama L.) constituted about 75% of total ®sh biomass, whereas piscivorous ®sh, such as pike (Esox lucius L.) and pikeperch (Stizostedion lucioperca L.) comprised only 10% (Hansson et al., 1998). For further details on the ®sh community see Persson (1997) and Persson & Hansson (1998). Annadotter et al. (1999) give a comprehensive account of the management history of the lake.
Fish removal Between the autumn of 1992 and spring of 1994, cyprinids (roach and bream) and small (< 150 mm) perch were removed at a rate of c. 0.5% of the population per day. All piscivorous ®sh (pike, pike-perch and large perch) were returned to the lake. Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
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In total, approximately 400 tons of ®sh were removed which is estimated to correspond to about 80% of the population of cyprinids and small perch (Hansson et al., 1998). For further details on ®sh removal see Persson & Hansson (1998).
during the study with respect to maximum Secchi depth and morphometry of the lake. Accordingly, no macrophytes were found outside this depth, except for single plants at one site that were found at 3.2 m in 1996.
Macrophyte surveys
Seed bank investigation
The macrophyte surveys were carried out in September from 1992 to 1997. In the ®rst year, the entire littoral zone was surveyed (visually) to assess the distribution of submerged macrophytes. From this investigation 10 sites around the lake were selected and revisited each year. Three sites were chosen because they constituted the small (< 100 m2) submerged macrophyte populations that existed prior to biomanipulation. The remaining seven sites were distributed between these three sites (Fig. 1). Macrophytes were sampled by inserting a PVC-tube (é 0.5 m) into the sediment, after which all aboveground biomass within the tube was collected with a rake. Because of the remarkably fast expansion of macrophytes into deeper water after the biomanipulation, the sampling method was changed at water depths greater than 1.7 m. At deep water (> 1.7 m), the macrophytes were collected from a boat with a rake, but without the tube, each sample covering about 0.1 m2. At each site, sampling was carried out along 50 m transects parallel to the shoreline (Fig. 1). Each 50 m transect was located at 0.1 m water depth intervals starting just outside the reed belts. At each water depth ®ve samples were taken randomly along the transect (Fig. 1). Sampling continued lakewards until no vegetation was found in any of the ®ve samples at three consecutive water depths. The greatest water depth with any submerged macrophytes was designated as outer water depth for each site. After sampling, each site was visually surveyed to determine if plants grew deeper than the sampling method could detect. This was noted separately but not used in the statistical analyses (but see Table 2). The plants were transported to the laboratory, dried (85 °C, 24 h) and weighed (DW). Cover was calculated as the percentage of samples that contained any submerged macrophytes up to 3 m water depth. Above-ground biomass at each site was calculated as the mean of all water depth intervals up to 3 m water depth for each year, which was proposed as a possible maximum potential of outer water depth
At each of the 10 sites, 10 sediment samples (top 5 cm) were taken in February 1994, with a sediment corer (é 7 cm) at 1.5 m water depth. The sediments were stirred and spread in containers (é 20 cm, h 15 cm), and immersed in 14 cm of aerated tap water. The containers were distributed randomly, amongst seed bank samples from other lakes, in a greenhouse with an air temperature of approximately 20 °C. The sediment samples were checked for germination of seeds once weekly. Seedlings were removed, counted and identi®ed. After 2 months the sediment was stirred again to bring potential non-germinated seeds to the sediment surface. The experiment lasted for 5 months.
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
Grazing experiments In 1993 (10±14 May), two sites were chosen with and without submerged macrophytes the previous year, to ®nd if waterfowl grazing could prevent or delay the re-colonization of submerged macrophytes after the biomanipulation. At each site, 20 cages were placed in the sediment at 0.8 m water depth. All cages were covered with metal net (mesh size 19 cm) and extended 30 cm above the water surface. At each site, 20 control areas were marked with wooden sticks. The experiment ended on 26 August. In each cage and control a PVC-tube (é 0.5 m) was inserted in the sediment and the macrophytes were collected with a rake. The plants were transported to the laboratory, dried (85 °C, 24 h) and weighed (DW).
Statistical analyses Biomass was log(x + 1) transformed and percentage cover was arc sin transformed, to meet assumptions of normality. All analyses were performed in SuperANOVA (Abacus Concepts Inc., Berkeley, CA, U.S.A., 1989). Because of the different sampling methods, the biomass data above 1.7 m water depth from the macrophyte survey was treated separately.
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Fig. 1 Depth curves (1±5 m) and sampling sites (black circles) in Lake FinjasjoÈn. A hypothetical sampling site is also shown, with seven transects (0.1±0.7 m) and ®ve samples along each transect (white circles).
Results Macrophyte surveys The vegetation expanded from small populations at three of the ten sites in 1992 to be present at all sites in 1995 (Table 1). The total above-ground biomass increased each year from 1993 to 1996 (P < 0.05), but decreased again in 1997 (P < 0.05) (Fig. 2). There was a signi®cant increase in cover from 1992 to 1996 and a
decrease in 1997 (P < 0.05) (Fig. 2). The decrease in biomass and cover in 1997 were mainly attributed to the disappearance of E. canadensis (Fig. 3, Table 1). The response to biomanipulation differed largely between the different species (Fig. 3). Myriophyllum spicatum and E. canadensis responded strongly and their biomass increased signi®cantly (Fig. 3). After 4 years, these two species had increased the aboveground biomass and cover by more than one order of Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
Dynamics of submerged macrophyte populations Table 1 Occurrence of different submerged macrophyte species at the sites during the years 1992±97 in Lake FinjasjoÈn. Ð = absent from all the 10 sites, 10 = present at all the 10 sites
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Year Sites
1992
1993
1994
1995
1996
1997
Myriophyllum spicatum Elodea canadensis Potamogeton perfoliatus E. acicularis P. pectinatus P. crispus P. praelongus P. obtusifolius
3 1 2 1 Ð Ð Ð 1
4 3 2 1 1 1 1 1
9 9 2 1 1 1 Ð 1
10 10 2 1 Ð Ð Ð Ð
10 10 2 1 Ð Ð Ð Ð
10 Ð 2 1 Ð Ð Ð Ð
Total plants
3
6
9
10
10
10
Fig. 2 Mean (1 SD, n 10) above-ground biomass (< 1.7 m black bars, > 1.7 m white bars) and cover (black squares) of the total submerged vegetation in areas above 3 m water depth at the 10 sites during the period 1992±97. Bars or squares that share a common letter are not signi®cantly different using A N O V A ; Fischer's PLSD test, P < 0.05 (within the groups; cover, biomass < 1.7 m, biomass > 1.7 m).
magnitude. The M. spicatum biomass was still high in 1997, but the E. canadensis population totally disappeared from all the sites. Potamogeton perfoliatus biomass increased after the biomanipulation, although no signi®cant differences between years were found, but no new sites were colonized (Table 1). Potamogeton obtusifolius was seemingly negatively affected and disappeared 3 years after the biomanipulation (Table 1). The small population of E. acicularis found at one site did not show any changes in biomass, cover or outer depth. Three Potamogeton species (P. crispus, P. pectinatus and P. praelongus) appeared (but with very low biomass) after the biomanipulation at one site, but disappeared within 2 years (Table 1). Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
Outer water depth also increased signi®cantly and remained high in 1997 (Fig. 4). Single plants occasionally grew deeper than the recorded outer depth but were very sparse and thus not detected with the sampling method used here (Table 2). Myriophyllum spicatum and E. canadensis grew deepest, they were regularly found at 2.8 m and single plants occurred up to 3.2 m in 1996 (Table 2). The depth of maximum above-ground biomass also increased after the biomanipulation (Fig. 5, Table 3). Macrophyte variables (above-ground biomass and cover) were positively correlated with Secchi depth, and negatively related to chlorophyll a, total phosphorus and PO4±P (Fig. 6). Total species richness increased after biomanipulation (from ®ve to eight) because of the appearance of P. crispus, P. pectinatus and P. praelongus (Table 1). However the species richness decreased after 1993. In 1997, only three species were found at the sites (M. spicatum, P. perfoliatus and E. acicularis) (Table 1). Mean species number at the sites also changed after biomanipulation, with an initial increase and thereafter a decrease (Fig. 7). During the increase there was a large variation between the sites, this being attributed to some sites with four or ®ve species, and some sites with no species at all. As the total species number decreased and the few remaining species colonized more sites, the variation in species number showed a large decrease (Fig. 7).
Seed bank investigation There were almost no viable seeds of submerged macrophytes. The only germinating species were three individuals of Chara globularis, and one individual of P. crispus (growing from a turion).
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Fig. 3 Mean (1 SD, n 10) aboveground biomass (< 1.7 m black bars, > 1.7 m white bars) of the four most common submerged species in areas < 3 m water depth in the lake during the period 1992±97. Bars that share a common letter are not signi®cantly different using A N O V A ; Fischer's PLSD test, P < 0.05 (capital letters biomass > 1.7 m).
Grazing experiments No effect of bird grazing on the submerged vegetation was found (two-way A N O V A ) for the treatment (exclosure) (F1,76 0.414, P > 0.05) or between sites (with or without macrophytes the previous year) (F1,76 0.725, P > 0.05). Furthermore, there was no interaction between factors (enclosure ´ site) (F1,76 0.051, P > 0.05).
Discussion This study showed that submerged macrophytes have a large capability for rapid recolonization if conditions improve, even in large lakes as FinjasjoÈn (11 km2). It seems possible that the increased Secchi depth, during and after biomanipulation (1992±94), caused the initial increase in submerged vegetation. The initial increase in Secchi depth after biomanipulation was probably caused by the increase in zooplankton biomass (Hansson et al., 1998) and a subsequent increase in grazing pressure on phytoplankton. Even after the biomanipulation, however, the Secchi depth
continued to increase (1994±96). Data on the zooplankton in FinjasjoÈn showed an increase in Daphnia the year after the biomanipulation (i.e. 1994) (Annadotter et al., 1999). However, unpublished data on zooplankton between 1994 and 1997, showed that after the initial increase there was a decrease in large Daphnia (H. Annadotter pers. comm.). Thus the increase in Secchi depth after 1994 is not likely to be caused by zooplankton grazing. This implies that the increase in submerged vegetation is the cause, rather than the effect, of the increased Secchi depth after 1994. The disappearance of E. canadensis, and the subsequent decrease in Secchi depth in 1997 further strengthens the argument that submerged vegetation is important for the turbidity. If Secchi depth was the causal factor, other species should decrease as well. As this did not happen it is possible that E. canadensis disappeared for other reasons (see below) and that the subsequent lower macrophyte biomass in the lake caused the decrease in Secchi depth. Our results agree with the conjecture that alterations in the food chain (mostly pelagic processes) may be viewed as triggers that initiate Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
Dynamics of submerged macrophyte populations
Fig. 4 Mean (1 SD, n 10) outer depth of the submerged vegetation at the 10 sites during the period 1992±97. Squares that share a common letter are not signi®cantly different using A N O V A ; Fischer's PLSD test, P < 0.05.
other processes important for the stabilization of a lake in the clear-water state (littoral and benthic processes) (Hansson et al., 1998). We suggest that an important mechanism behind the stabilizing effects of submerged macrophytes is nutrient uptake by periphyton (Strand, Johansson & Weisner, 1998), and not nutrient uptake directly by submerged macrophytes as has been suggested (Ozimek et al., 1990). Submerged macrophytes mostly derive their nutrients directly from the sediment (Carignan & Kalff, 1980), and are therefore not directly competing with the phytoplankton community for nutrients. However, an increase in submerged
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vegetation leads to increased surface areas available for periphyton production, and as periphyton derive their nutrients from the water (Cattaneo & Kalff, 1979), an increased periphyton production may cause increased nutrient competition between phytoplankton and periphyton (Strand et al., 1998). Increased denitri®cation in the periphyton community can further decrease nutrient availability for the phytoplankton (Weisner et al., 1994). Calculations using data on periphyton dry weight per macrophyte leaf area from FinjasjoÈn during the period June±August (Strand, 1999b; J.A. Strand & S.E.B Weisner, unpublished data), show that large amounts (up to 3 t) of phosphorus are bound in periphyton biomass in years when macrophytes are abundant. Thus, a large decrease in the submerged macrophyte biomass (as between 1996 and 1997) could lead to increased P availability for the phytoplankton because of released nutrient competition from periphyton, and subsequently a lower Secchi depth. Between 1996 and 1997, total phosphorous increased from 0.031 to 0.049 mg L±1, and chlorophyll a increased from 19 to 28 lg L±1 (data from management reports). On senescence, periphyton communities settle of on the sediment surface, are incorporated in the sediment and decomposed, and nutrients are utilized by the benthic microbial communities and submerged plants. However, other factors such as uptake by benthic algae and bacteria are also important for the nutrient cycle in eutrophic lakes (Hansson, 1989; Van Luijn et al., 1995; Jeppesen et al., 1998). The relative importance of these mechanisms needs, however, to be clari®ed. It is possible that management measures other than biomanipulation caused the observed changes in
Table 2 Maximum outer water depth (cm) of the submerged macrophytes in the sampling programme during the years 1992±97 in Lake FinjasjoÈn. () = Visual observations of deeper-growing plants, not detected in the sampling Year Sites
1992
1993
1994
1995
1996
1997
Myriophyllum spicatum Elodea canadensis Potamogeton perfoliatus E. acicularis P. pectinatus P. crispus P. praelongus P. obtusifolius
60 (70) 30 30 (50) 30 Ð Ð Ð 40
80 (90) 90 40 (70) 30 50 60 80 40
220 (250) 200 (230) 80 (110) 30 60 60 Ð 30
250 250 (260) 80 (100) 30 Ð Ð Ð Ð
280 (320) 280 (300) 90 (120) 30 Ð Ð Ð Ð
270 (300) Ð 100 (120) 30 Ð Ð Ð Ð
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
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Fig. 5 Mean above-ground biomass at different water depths in Lake FinjasjoÈn during the period 1992±97 (n 10). Black bars represent biomass above 1.7 m water depth and white bars represent biomass below 1.7 m (different sampling methods used).
Year Sites
1992
1993
1994
1995
1996
1997
Myriophyllum spicatum Elodea canadensis Potamogeton perfoliatus E. acicularis P. pectinatus P. crispus P. praelongus P. obtusifolius
50 30 30 20 Ð Ð Ð 20
80 80 40 20 50 60 80 30
150 100 60 20 50 60 Ð 20
160 120 60 20 Ð Ð Ð Ð
200 180 80 20 Ð Ð Ð Ð
190 Ð 80 20 Ð Ð Ð Ð
FinjasjoÈn. Improved waste water treatment and within-lake sediment removal (Annadotter et al., 1999), might have lag-phase effects that partly explain the improved conditions. However, we suggest
Table 3 Depth (cm) of maximum aboveground biomass of the submerged macrophytes during the years 1992±97 in Lake FinjasjoÈn
that the increase in submerged macrophytes is an important factor for the long-term improvement in water clarity and the underlying mechanisms should be further investigated. Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
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Secchi depth (m)
2.5 96
2
96 97
95
1.5
97 95
1
94 94 93 92
0.5
93 92
0 93 92
Chl a (µg L–1)
60
93 92
50 94
40
94
30 95 97
20
95 97 96
96
10
Tot-P (mg L–1 )
92
92
0.2 0.15
93
93
0.1 94 0.05
95 97
PO4 -P (mg L –1 )
0
Fig. 6 Relation between two submerged macrophyte variables (above-ground biomass and cover), and Secchi depth, chlorophyll a, Tot-P and PO4±P for the years 1992±97. Tot-P, PO4±P, Secchi depth and chlorophyll a are summer means (data from management reports).
94
97 95
96
92
96
92
0.05 0.04 0.03 0.02 0.01
93
95
94
93
95 0
0
25
50
97
96 75
100
Biomass (g DW)
The reason for the rapid spread of E. canadensis and M. spicatum is probably because of their fragmentative (vegetative) dispersal, that can result in rapid colonization of new areas during one season (Kimbel, 1982). Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
94 97 96
0
20
40
60
80
Cover (%)
Even in a large lake as FinjasjoÈn where dispersal distances by necessity are great, the vegetative spread is apparently very effective when colonizing new areas. The reason for the collapse of E. canadensis is
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Mean species richness
4 3 2
b ab
b
b
a a
1 0 –1 92 93 94 95 96 97 Year
Fig. 7 Changes in mean species richness (1 SD, n 10) in Lake FinjasjoÈn during the period 1992±97. Squares that share a common letter are not signi®cantly different using A N O V A ; Fischer's PLSD test, P < 0.05.
more obscure, but two consecutive strong winters 1995±96 and 1996±97 with a prolonged ice cover could be an explanation. This species lacks a dormancy mechanism (Haag, 1979), and is therefore dependent on at least some photosynthetically active radiation reaching the plant even during winter. Elodea canadensis is known to have a cyclic pattern, with sudden disappearance after some years of rapid growth (Lauridsen et al., 1994). Rùrslett (1986) tested the enrichment hypothesis, but found the opposite trend, e.g. that during Elodea's build-up, water quality (i.e. nutrients, algal blooms) improved whereas during Elodea's dieback the system deteriorated. He concluded that an alternative hypothesis is clearly needed (Rùrslett, 1986). Our results indicate that increased periphyton production and biomass build-up can be one explanation for the positive effects of submerged macrophytes in lake ecosystems. The population of P. perfoliatus showed a slower and weaker positive response to biomanipulation, both temporally and spatially, compared with E. canadensis and M. spicatum. This species does not have the capability of fragmentation or turion formation, but depends on seeds for long-distance dispersal (i.e. to new sites in the lake). Conversely, vegetative dispersal by rhizomes was probably the main mechanism for the within-site increase in biomass, cover and increased depth distribution of this species.
The reason for the decrease in species number could be light competition from E. canadensis and M. spicatum, as the Potamogeton species are weak competitors compared with M. spicatum and E. canadensis (Madsen, Hartleb & Boylen, 1991a). In particular, M. spicatum concentrates on the major part of the above-ground biomass near the water surface (Adams, Titus & McCracken, 1974), and is thus a strong competitor for light. A number of papers have reported a decrease in other species when M. spicatum and E. canadensis have invaded (Nichols & Shaw, 1986; Madsen, Eichler & Boylen, 1988; Madsen et al., 1991a,b). However, the lack of increase in species number after the disappearance of E. canadensis in 1997 implies that other factors apart from competition also affected species richness. A viable seed bank has been proposed as a prerequisite for the success of biomanipulation projects (i.e. to get a rapid recolonization of submerged macrophytes) (Hosper & Meijer, 1992). In FinjasjoÈn, however, the macrophytes responded fast without any apparent viable seed bank. The experiment was conducted simultaneously with samples from other lakes, using the same water and greenhouse conditions. As there was a high germination rate in sediments from the other lakes, it is not possible that the lack of germination from FinjasjoÈn was caused by experimental error. The occurrence of charophyte oospores in the seed bank is in accordance with results from other lakes, where we found large numbers of germinating charophyte seedlings although charophytes were absent in the vegetation (J.A. Strand & S.E.B Weisner, unpublished data). Charophytes have been previously abundant in the lake (Almestrand & Lundh, 1951). We did not observe any effect of waterfowl grazing on the establishment of submerged vegetation, as has been found in other studies (Lauridsen et al., 1993). The reason might be a too low density of herbivorous birds; bird numbers increased substantially (data on bird counts by local ornithology clubs), but only after the increase in submerged vegetation. FinjasjoÈn is a relatively isolated lake and the lack of nearby lakes with submerged macrophytes and dense waterfowl populations might explain the low grazing pressure during the ®rst years of re-colonization. It is, however, dif®cult to draw ®rm conclusions from one single exclosure experiment as a number of factors can in¯uence the bird's behaviour. Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1397±1408
Dynamics of submerged macrophyte populations In conclusion, our study shows that submerged vegetation can rapidly recolonize also large lakes from very small plant populations still present in the turbid state, after an initial increase in Secchi depth. Species that spread by fragments will increase rapidly and probably outcompete other species. Furthermore, the submerged vegetation and Secchi depth increased further also after the initial increase in Secchi depth, despite low densities of Daphnia. One explanation is to implement feed-back mechanisms where increased macrophyte biomass leads to increased periphyton production and a subsequent nutrient limitation of phytoplankton, which increase Secchi depth and lead to a further increase in submerged vegetation.
Acknowledgments The local authorities of HaÈssleholm kindly provided logistic support at Lake FinjasjoÈn and supported us with background data. HaÊkan Sandsten, Peder Eriksson, Teresa Soler, MaÊns Denward, Viveka Vretare and Jonas Svensson were helpful during sampling and other ®eldwork. Two anonymous reviewers gave valuable comments on earlier versions of the manuscript. This study was partly done within the Swedish Water Management Research Program (VASTRA) with ®nancial support from the Swedish Foundation for Strategic Environmental Research (MISTRA).
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