Post on 16-May-2023
PRIMARY RESEARCH PAPER
Shifts in water quality in a drinking water reservoirduring and after the removal of cyprinids
Tiia Pedusaar • Ilkka Sammalkorpi •
Arto Hautala • Jaana Salujoe •
Ain Jarvalt • Margus Pihlak
Received: 14 September 2009 / Revised: 28 February 2010 / Accepted: 8 March 2010 / Published online: 30 March 2010
� Springer Science+Business Media B.V. 2010
Abstract Lake Ulemiste, the drinking water reser-
voir of Estonia’s capital city Tallinn, was biomanip-
ulated by manual removal of cyprinids in 2004–2006
and its impact on water quality in the vegetation
period was studied. A total biomass of 156 tonnes
corresponding to 160 kg ha-1 of fish, predominantly
cyprinids, were removed. A decline in the unit
catches of fishing was observed. The removed fish
biomass versus phosphorus concentration of the lake
was considered sufficient to reduce the impact of
cyprinids on water quality. The phosphorus removed
within fish biomass corresponded to 38 lg l-1 and
21% of the external phosphorus load of the fishing
period. The mean total phosphorus concentration
dropped from [50 to B36 lg l-1. However, the
densities of planktivorous young-of-the-year percids
remained high and the role of zooplankton grazing in
improving water quality was found non-significant or
transient. The cladocerans biomass decreased and the
small-sized Daphnia cucullata remained almost
the only daphnid in Lake Ulemiste during and after
the manipulation. Predomination of filamentous
cyanobacteria was replaced by a more diverse
phytoplankton composition and co-domination of
micro- and pico-sized colonial cyanobacteria during
summer. Mean phytoplankton biomass decreased
from 15 to 6 mg l-1 primarily as a result of decreased
in-lake TP availability. The Secchi disc transparency
increased only in May 2005–2007. The effects of
coincidental events, a decline of external loading of
phosphorus and a simultaneous flushing induced by
heavy rainfall, on lake water quality are discussed
with some implications to the future management of
the reservoir.
Keywords Drinking water reservoir �External loading � Fish removal � Heavy rainfall �Restoration � Water quality
Handling editor: P. Noges
T. Pedusaar (&)
Department of Environmental Engineering, Tallinn
University of Technology, Ehitajate tee 5, 19086 Tallinn,
Estonia
e-mail: tiia@mtb.ee
I. Sammalkorpi
Finnish Environment Institute, P. O. Box 140, 00251
Helsinki, Finland
A. Hautala
Department of Biological and Environmental Sciences,
University of Jyvaskyla, P. O. Box 35, 40351 Jyvaskyla,
Finland
J. Salujoe � A. Jarvalt
Centre for Limnology, Estonian University of Life
Sciences, Rannu, 61101 Tartu, Estonia
M. Pihlak
Department of Mathematics, Tallinn University of
Technology, Ehitajate tee 5, 19086 Tallinn, Estonia
123
Hydrobiologia (2010) 649:95–106
DOI 10.1007/s10750-010-0231-x
Introduction
Reduction of excessive external nutrient loading is the
first step in management and indispensable prerequi-
site for recovery of eutrophic lakes and reservoirs
(Vollenweider, 1976). Yet, even after successful
loading reduction, recovery may be slow as a result
of chemical or biological resistance of the ecosystem
(Benndorf, 1990; Jeppesen et al., 1991). To overcome
biological resistance in the waterbody and accelerate
the recovery of a lake, various biomanipulation
methods have been developed (e.g. Søndergaard
et al., 2001), one of these being selective removal of
planktivorous and benthivorous cyprinids based on
findings of Hrbacek et al. (1961) and Shapiro (1980).
A major indicator of successful biomanipulation is
a significant improvement in water transparency,
achieved through top-down and/or bottom-up control
(Carpenter et al., 1987). Reducing planktivorous fish
reduces predation pressure on zooplankton leading to
stronger top-down control on phytoplankton. Reduc-
ing benthivorous fish decreases the amount of
nutrients available for phytoplankton from sediment
resuspension (e.g. Horppila & Kairesalo, 1990;
Scheffer et al., 2003).
During eutrophication, lakes may change from a
clear water, macrophyte dominated state to a turbid,
phytoplankton dominated state. Shifts between clear
and turbid states may be due to different mechanisms,
such as drastic natural events (e.g. extreme weather
conditions) or a stepwise change due to restoration
measures, including biomanipulation (e.g. Scheffer,
1998; Noges & Noges, 1999; Hargeby et al., 2007;
van Nes et al., 2007).
Lake Ulemiste functions as the drinking water
reservoir for the capital of Estonia, Tallinn (0.4 million
inhabitants). Since the beginning of the 1990s, the
previously high external nutrient loading to the lake
decreased, mainly as a result of declining inflow due to
the city’s reduced water consumption. The phosphorus
(PO4-P) load to the lake decreased from 0.38 g m-2
year-1 in 1991 to 0.18 g m-2 year-1 in 2003.
Although the external loading had steadily decreased,
there was no constant downward trend in water
turbidity (Reinart & Pedusaar, 2008), and cyanobac-
teria continued to dominate the lake’s phytoplankton
community (Trei, 2002). The water treatment technol-
ogy of the plant is adjusted to the water quality in the
lake, therefore, better raw water quality, especially in
the summer months, would allow more cost-efficient
drinking water production.
In 2004, biomanipulation as an in-lake restoration
measure was initiated in Lake Ulemiste to speed its
recovery. Pre-manipulation test fishing showed a high
proportion of bream (Abramis brama (L.)) inacces-
sible for gape limited piscivores and a high density of
YOY percids, perch (Perca fluviatilis (L.)) and
pikeperch (Sander lucioperca (L.)) in the lake
(Pedusaar et al., 2008). Expectations based on
positive linear relationship between phytoplankton
abundance measured as biomass or chlorophyll a
(Chl a) and total phosphorus (TP), showed sufficient
grounds for fish removal as it was hypothesized that it
will primarily reduce nutrient concentrations (avail-
ability of sediment phosphorus) and enhance also
zooplankton grazing (Pedusaar et al., 2008). There-
fore, fish removal was focused on benthivorous
bream and omnivorous roach (Rutilus rutilus (L.)).
In this article, we analyse the changes of nutrients,
water transparency, phyto- and zooplankton in Lake
Ulemiste (Estonia) during the years affected by the
manual removal of cyprinids (2005–2007) compared
with the pre-manipulation period (2000–2004).
Material and methods
Study area
Ulemiste, the fourth largest lake in Estonia
[9.75 km2, mean depth 3.4 m; maximum depth
5.2 m; total volume at normal pool level (36.6 m
above the sea level (m.a.s.l.) according to the Baltic
system) 32 mm3] is situated on the southernmost
border of Tallinn. A map of the lake is shown in
Pedusaar et al. (2008). Lake Ulemiste is a shallow,
polymictic hardwater lake. At present, the water level
is controlled by the Water Treatment Plant (WTP)
and the mean water residence time (WRT) is
approximately 1 year. More about the lake, its biota
and catchment area can be found in Erm et al. (2001),
Faulkner et al. (2003) and Pedusaar et al. (2008).
Sampling and analyses
Most of the studied water quality parameters in the
lake and its inflows were sampled once a week from
May to October in 2000–2007. Routine sampling of
96 Hydrobiologia (2010) 649:95–106
123
TP and TN began in February 2001, Secchi trans-
parency was measured since June 2003, and Chl a
since July 2003. TP and TN were analysed according
to ISO standards. Routine phytoplankton samples
were preserved with acid Lugol solution, settled
and counted according to the Utermohl technique
(Utermohl, 1958) using an inverted microscope
(magnification 10 9 40). Cell/colony numbers were
converted to biomass by stereometrical formulae as
described by Blomqvist & Herlitz (1998). Pico- and
micro-size cyanobacteria colonies were not singled
out and identified in the routine counting process but
were identified, according to Komarek & Anagnos-
tidis (1999), in random qualitative samples using a
Zeiss Axiovert 100 microscope (magnification 10 9
100). Chl a was determined spectrophotometrically
after ethanol extraction at room temperature and using
the equations of Jeffrey & Humphrey (1975). Zoo-
plankton samples were filtered through a plankton net
(mesh size 25 lm) and counted using a stereomicro-
scope. Zooplankters were divided into three groups:
Cladocera, Copepoda and Rotifera. Since September
2003, measurements and identification up to species
level started. The wet weight of a specimen was calcu-
lated on the basis of its length using Ruttner-Kolisko
(1977) formulas for rotifers, and Studenikina & Cher-
epakhina (1969) and Balushkina & Winberg (1979)
formulas for cladocerans and copepods. The filtering
rate of zooplankton was estimated using the regression
equation for cladocerans by Knoechel & Holtby (1986).
To enable an insight to magnitude of internal
processes, the mass balance calculations of TP were
carried out using the equation given by Cooke et al.
(1993):
TPsed ¼ TPin � TPout � DTP;
where TPsed is net internal budget, TPin is external
load, TPout is outflow loss and DTP reflects the
changes in water column TP storage over time. Water
balance calculation of Lake Ulemiste (Pedusaar et al.,
accepted) was the basis for the mass balance calcu-
lation indicated here. Calculations were made on a
monthly basis but the results are shown on an annual
basis. Atmospheric loading and exfiltration as sources
of minor importance in the water balance (Pedusaar
et al., accepted) were omitted in the mass balance
study. The WRT was calculated by dividing the lake
volume by the total output.
Statistics
Differences in water quality parameters of the
vegetation period between the pre-manipulation
(2000–2004), manipulation (2005 and 2006) and
post-manipulation (2007) period were compared
using one-way ANOVA with post hoc test of
Bonferroni. As the amount of data in different
periods was different, data were bootstrapped.
Although fish removal started already in 2004, we
included this year into the pre-manipulation period
(2000–2004) since 75% of the catch in 2004 was
made at the end of the vegetation period (October and
November). Univariate and multivariate regression
analysis were applied to test relationships. Data
were ln transformed when necessary. The pro-
gram SYSTAT version 8.0 was used for statistical
analysis.
Results
Fish removal
The total biomass of fish removed in 2004–2006
was 156 tonnes, corresponding to 160 kg ha-1. Total
catches during the 3 years were 35, 92 and
33 kg ha-1, respectively. The catch was dominated
by bream (55%) and roach (26%). The biomass of fish
removed in 2005 was close to the average target level
calculated from the TP concentration of the water of
successful case studies (Jeppesen & Sammalkorpi,
2002) suggesting that reduction should have been
sufficient to influence the phosphorus concentration of
Lake Ulemiste. The mean biomass removed from the
area of the seine hauls between July 2005 and 2006
when fishing effort was comparable, diminished from
95.7 kg ha-1 (±SE 9.1 kg; n = 27) to 50.1 kg ha-1
(±3.9 kg; n = 38). Since the fish removal was
selective for cyprinids, the high densities of young-
of-the-year (YOY) percids observed in 2003
(\10,000 ind. ha-1, Pedusaar et al., 2008) were not
affected. Median catch per unit effort (CPUEn) of
littoral YOY perch in Nordic multimesh gillnets
varied from 14 to 83 ind. in 2003–2007, being the
highest in 2006. Results on the fish stock changes will
be published in a separate paper.
Hydrobiologia (2010) 649:95–106 97
123
Hydrology
The mean WRT was approximately 1 year (variation
from 1.0 to 1.4 year) in the period 2000–2007. The
year 2004 was very wet (903 mm) compared to the
common mean annual precipitation (568 mm) in
Estonia. During a heavy rainfall in Tallinn on 28–29
July 2004 (week 31), the total amount of precipitation
was 145 mm within 48 h (Matlik & Post, 2008),
accounting for 16% of the annual precipitation. Its
subsequent flushing effect reduced the mean annual
WRT to 0.6 year (minimum 200 days) for 2 weeks
immediately after the rainfall.
Mass balance of TP and in-lake nutrients
The annual external TP loading fluctuated from 0.13
to 0.40 g TP m-2 y-1 in 2001–2007, being the
lowest in 2006–2007 (Table 1). External load of TP
to the lake was always higher than the outflow of TP
during observed years. Only in 2002 and 2005 did the
release of phosphorus exceed the rate of sedimenta-
tion in the lake. Assuming that 0.8% of the wet mass
of fish is phosphorus (Schreckenbach et al., 2001), a
total of 1.2 tonnes of fish-bound phosphorus was
removed in 2004–2006 (Table 1). This represents
21% of the external phosphorus loading in 2004–
2006. The losses of fish-bound phosphorus per
volume were 9, 21 and 8 lg l-1 in 2004, 2005 and
2006, respectively.
In 2005, the mean in-lake TP for the vegetation
period was significantly higher than during the pre-
manipulation period (Table 2), probably as a result of
a high net internal loading (Table 1). By contrast, in
2006 and 2007, the mean TP for May–October was
almost 40% lower than the pre-manipulation period
mean (Table 2). Mean in-lake TN showed an about
25% decline from the pre-manipulation level
(Table 2). In 2005, the mean TN:TP ratio for May–
October was significantly lower than the pre-manip-
ulation period mean but was significantly higher in
2006 and did not differ significantly from pre-
manipulation period ratio in 2007 (Table 2).
Phytoplankton and Chl a
The May–October mean total phytoplankton biomass
and Chl a were significantly lower in 2005–2007
compared to the pre-manipulation period (Table 2).
The dominance of cyanobacteria ([50% of total
phytoplankton biomass) was broken in August 2004
after heavy rainfall, with the emergence of diatoms
(Synedra spp., Asterionella formosa Hass. and uni-
cellular centric species), cryptophytes (Cryptomonas
spp., Rhodomonas spp.) and chlorophytes (Scenedes-
mus spp., Pediastrum spp.) (Fig. 1). Colonial cyano-
bacteria from the bloom-forming genus Microcystis
emerged with non-bloom-forming picocyanobacteria
(e.g. Aphanocapsa, Cyanodictyon) some weeks ear-
lier (Fig. 2a). In July 2005, cyanobacteria dominated
again (Fig. 1) but the typical filamentous species
(Limnothrix redekei (van Goor) Meffert, Aphanizom-
enon skujae Kom.-Legn. & Cronb., Planktothrix
agardhii (GOM.) Anagn. & Kom., Planktolyngbya
limnetica (Lemm.) Kom.-Legn.) shared the habitat
with the colonial forms mentioned above (Fig. 2a).
A shift from the dominance of filamentous cyano-
bacteria to co-domination with colonies and a decline
in the biomass of the dominant species L. redekei,
were evident in May–October 2004–2007 [Fig. 2a;
Pedusaar et al. (2008, Fig. 2a)].
The role of diatoms, chloro, crypto-, and chryso-
phytes (Dinobryon spp.) increased especially in the
phytoplankton community in May 2005–2007 coin-
ciding with higher Secchi transparency in the lake
(Fig. 1). The proportion of phytoplankton species
other than cyanobacteria in the total phytoplankton
biomass varied between 1 and 72% in May 2000–
2004 and between 71 and 95% in May 2005–2007.
Table 1 Mass balance of TP of Lake Ulemiste in 2001–2007
Year TPin TPout TPsed
kg y-1 g m-2 y-1 kg y-1 g m-2 y-1 kg y-1
2001a 1,500 0.16 948 0.10 ?659
2002 2,310 0.24 1,440 0.15 -105
2003 3,830 0.40 1,419 0.15 ?2,610
2004 2,500 0.26 1,100
(?298b)
0.15 ?2,306
2005 2,000 0.21 1,172
(?685b)
0.20 -1,513
2006 1,300 0.14 636 (?257b) 0.10 ?1,243
2007 1,260 0.13 622 0.10 ?1,246
TPin—external load; TPout—outflow loss; TPsed—net internal
budgeta Mass balance without January and Februaryb Fish-bound phosphorus
98 Hydrobiologia (2010) 649:95–106
123
Zooplankton
The mean zooplankton abundance and biomass were
significantly lower during the vegetation periods in
2005–2007 compared to the pre-manipulation period
(Table 2). Rotifers dominated ([50% of the total
zooplankton abundance) during and after the bioma-
nipulation as they did in 2000–2003 (Pedusaar et al.,
2008) although their abundance decreased signifi-
cantly in 2005–2007 (Table 2). The only exception
occurred immediately after the heavy rainfall in 2004
when the dominance of Bosmina c. coregoni Baird and
Table 2 Water quality parameters (mean ± SE) from May to October during pre-manipulation period (2000–2004), fish removal
(2005 and 2006), and a year after the intervention (2007) in Lake Ulemiste
Parameter 2000–2004
n = 32–138
2005
n = 26–27
2006
n = 26–27
2007
n = 26–27
TP (lg l-1)a 48 ± 1 54 ± 2 31 ± 2 36 ± 2
TN (lg l-1)a 1494 ± 40 1309 ± 59 1082 ± 46 1214 ± 136
TN:TP 34 ± 1 26 ± 2 38 ± 3 37 ± 4ns
Chl a (lg l-1)b 30 ± 2 23 ± 2 20 ± 2 21 ± 2
Phytoplankton biomass (mg l-1) 15 ± 1 9 ± 2 8 ± 1 6 ± 1
Zooplankton biomass (mg l-1)c 0.858 ± 0.184 0.586 ± 0.076 0.285 ± 0.061 0.236 ± 0.039
Zooplankton abundance (million ind. m-3) 0.589 ± 0.057 0.344 ± 0.038 0.245 ± 0.025 0.151 ± 0.019
Cladocerans biomass (mg l-1)c 0.570 ± 0.147 0.287 ± 0.048 0.165 ± 0.036 0.189 ± 0.038
Rotifers abundance (million ind. m-3) 0.486 ± 0.055 0.286 ± 0.033 0.218 ± 0.023 0.122 ± 0.019
According to one-way ANOVA test results, differences of water quality parameters in 2005, 2006 and 2007 compared to pre-
manipulation period were all significant (P \ 0.05), except TN:TP ratio in 2007
ns non-significant differencea TP and TN measurements are available since 2001b Chl a measurements started since July 2003c Zooplankton biomass measurements with species identification started in September 2003
Fig. 1 Phytoplankton composition (% of total biomass, columns) and Secchi disc (monthly mean, cm, open diamond; filled diamonddenote the May) during May–October in Lake Ulemiste in 2000–2007
Hydrobiologia (2010) 649:95–106 99
123
(a) (b)
Fig. 2 a Proportions of filaments and colonies in cyanobac-
teria biomass in Lake Ulemiste in May–October 2004–2007.
Absence of columns denotes lack of cyanobacteria.
b Proportion of main cladocerans in total cladocerans biomass
and their mean filtering rate (% of the lake volume, open rings)
in May–October 2004–2007 in Lake Ulemiste. Absence of
columns denotes lack of cladocerans
100 Hydrobiologia (2010) 649:95–106
123
Daphnia cucullata Sars accounted for [50% of total
zooplankton abundance in weeks 31–35. This density
peak also coincided with the peak in cladoceran
filtering rate reaching 37% of the lake volume in week
31 in 2004 (Fig. 2b).
B. c. coregoni and C. sphaericus with D. cucullata
comprised major part of the cladoceran biomass
(Fig. 2b). Small-sized D. cucullata remained almost the
only daphnid in Lake Ulemiste during manipulation and
in the subsequent year. Daphnia galeata Sars appeared
only temporarily in autumn 2005 (0.14 mg l-1). There
was no increase in the mean length of the dominant
cladoceran species (D. cucullata 0.56 mm; B. c. coregoni
0.41 mm and C. sphaericus 0.30 mm) compared to their
size before manipulation neither did the cladocerans
filtering rate increase (Fig. 2b).
The predatory cladoceran Leptodora kindtii (Focke)
with peak abundance of 800 ind. m-3 appeared after
the heavy rainfall in 2004 (Fig. 2b). In 2005, Lepto-
dora was present occasionally but in the 24th week of
2006, Leptodora was the only cladoceran species
comprising 97% (200 ind. m-3) of the total zooplank-
ton biomass. In the following week, all cladocerans
disappeared but the lake’s common cladoceran com-
munity recovered within a few weeks (Fig. 2b).
Leptodora was not found at all during 2007.
Relationships of phytoplankton biomass and Chl a
with TP and Daphnia
Before fish removal, changes in TP explained 78% of
the variation of Chl a and 38% of that of phytoplank-
ton biomass (Pedusaar et al., 2008). During May–
October 2005–2007, univariate regression analyses
showed mainly significant though weaker effect of TP
on Chl a and phytoplankton biomass explaining again
better changes in Chl a than in phytoplankton biomass
(Table 3). The slopes of the regressions were smaller
than before fish removal (Table 3; Pedusaar et al.,
2008). The year 2005 was an exception as despite the
significant TP increase, phytoplankton biomass and
Chl a decreased, reflecting the importance of factors
other than TP. Impact of Daphnia on the variability of
phytoplankton biomass and Chl a was inconsistent
and mainly non-significant in 2005–2007.
Water transparency
Although the phytoplankton biomass and Chl a were
significantly lower during vegetation periods in
2005–2007 compared to the pre-manipulation period,
monthly means of Secchi disc readings did not show
any increase, except for May. In May 2005–2007, the
Table 3 Univariate and multivariate regressions indicating the relationships of TP (mg l-1), Daphnia biomass (mg l-1) and Chl a(lg l-1) with phytoplankton biomass (mg l-1), Chl a and Secchi transparency (cm)
Year Dependent variable/
independent variable
Intercept TP Daphnia Chl a r2
2005 Phytoplankton biomass 5.07ns 1.14* – – 0.06
6.07ns 1.42* -1.28ns – 0.02
Chl a 5.43** 0.80* – – 0.20
4.56** 0.56ns 1.10* – 0.34
Secchi transparency 6.88** – – -0.88** 0.81
2006 Phytoplankton biomass 7.72** 1.70* – – 0.27
6.24* 1.32* 4.65ns – 0.27
Chl a 6.68** 1.07** – – 0.47
5.74** 0.83** 2.96* – 0.55
Secchi transparency 2.65* -0.57* – -0.1ns 0.64
2007 Phytoplankton biomass 4.92* 1.01* – – 0.15
5.71* 1.22* -2.62ns – 0.09
Chl a 6.20** 0.98* – – 0.32
6.4** 1.03* -0.66ns – 0.26
Secchi transparency 5.87** – – -0.55** 0.69
n = 26–27
* P \ 0.05; ** P \ 0.001; ns not significant
Hydrobiologia (2010) 649:95–106 101
123
mean Secchi depth exceeded 1 m as it did not do
earlier (Fig. 1). Most of the variability of Secchi
transparency can be attributed to Chl a and, indi-
rectly, to TP in the lake (Table 3).
Discussion
Nutrient dynamics of the lake
A decline in in-lake TP has been observed in many
biomanipulation case studies (e.g., Hansson et al.,
1998; Jeppesen & Sammalkorpi, 2002; Søndergaard
et al., 2001), but as the external loading to Lake
Ulemiste decreased gradually at the same time when
the manual fish removal was expected to have an
impact, the question remains, which was the main
cause of the observed in-lake TP decrease in 2006
and 2007. Lake Vortsjarv is another extensively
studied large polymictic lake in Estonia, which has
several similarities with Lake Ulemiste in nutrient
dynamics, loading history, retention time as well as in
phytoplankton composition (Noges et al., 2004).
Comparing the mean TP values of Lake Ulemiste in
the period May–October 2006–2007 with those of
Lake Vortsjarv, the latter did not change (database of
The Estonian Environment Information Centre). Yet,
in 2000–2004, before the manipulation, the TP
concentrations in Lake Ulemiste (48 lg l-1) were
comparable to those of Lake Vortsjarv (50 lg l-1).
This also suggests that the TP decline by 20 lg l-1 in
Lake Ulemiste in 2006 and 2007 could result from
the fish removal. However, also the effect of lower
external loading was probably important since the in-
lake TP reached its lowest values in 2006 and 2007.
A similar combined effect of drought induced
reduction of external loading and fish removal has
earlier been reported from the mesotrophic Lake
Pyhajarvi in Finland (Ventela et al., 2007).
The in-lake TN had a slightly decreasing trend
during the pre-manipulation period (Pedusaar et al.,
2008) and continued to decrease in 2005–2007.
Despite this, TN remained high in Lake Ulemiste
(monthly means seldom below 1,000 lg l-1),
exceeding also the TN values in Lake Vortsjarv
(values seldom above 1,000 lg l-1). On the other
hand, higher TN but lower TP result in a higher
TN:TP ratio which, in turn, favours the development
of algal species other than cyanobacteria.
Changes in plankton, Chl a and water
transparency
Based on strong positive linear dependence of
phytoplankton biomass and Chl a on TP (Pedusaar
et al., 2008), we expected to find lower phytoplankton
biomasses and Chl a levels in 2006 and 2007 because
of lower in-lake TP. Nevertherless, the findings were
in line with those of others (Jeppesen et al., 2005;
Phillips et al., 2005), showing that the response of
summer and autumn plankton is most prone to delay
to decreased availability of nutrients in shallow lakes
in the early recovery phase. The decreased phyto-
plankton biomass in Lake Ulemiste resembles that of
the phytoplankton biomass in Lake Peipsi s.s. (Noges
et al., 2007; Laugaste et al., 2008), another well
studied lake in Estonia having moderately eutrophic
features (Laugaste et al., 2001).
The rapid change in phytoplankton composition
since week 32 in 2004 might be attributed solely to a
short-term destabilization of the water column due to
flushing as the nutrient concentrations showed no
decrease and the water temperature was near opti-
mum. It is likely that the wet summer offered
opportunities to other species, including colonial
cyanobacteria, and that the subsequent heavy rainfall
favoured their development. Cyanobacteria lost their
dominance for 11 months after the rainfall suggesting
the effectiveness of the flushing which has been
successfully used to reduce the amount of cyanobac-
teria, especially filamentous cyanobacteria in lakes
(Scheffer et al., 1997; Davis et al., 2003). Also the
temporary increase in filtering rate by zooplankton
community could play a role.
Small-sized algae with faster growth rates tend to
dominate in more rapidly flushed systems (e.g. Kalff,
2002) and the relative contribution of picoplankton to
total phytoplankton biomass increases in waterbodies
with lower trophic status (e.g. Voros et al., 1998;
Schallenberg & Burns, 2001). We suggest that the
observed emergence of picoplankton could be trig-
gered by the flushing effect, but its larger contribution
among the phytoplankton continued due to the
decreasing TP concentration in Lake Ulemiste. This
is also consistent with the observations of Raven
(1998) who stated that in low-resourced environ-
ments smaller cells are better able to acquire
resources and use them effectively in growth than
are larger cells.
102 Hydrobiologia (2010) 649:95–106
123
Slow growing Limnothrix redekei, the main dom-
inant in the phytoplankton community of Lake
Ulemiste (Trei, 2002; Pedusaar et al., 2008) and the
indicator species of hypertrophy in Estonian lakes
(Laugaste et al., 2001) nearly collapsed suggesting
changes in the lake’s ecosystem. Limnothrix redekei
is a successful competitor in nutrient rich and low-
light conditions (e.g. Nicklisch & Kohl, 1989) but as
light conditions in the key period, i.e. in May
improved and TP decreased in Ulemiste, it may be
the reason why L. redekei lost its advantage among
other phytoplankton species giving rise to fast
growing chroococcal species.
Higher diversity in phytoplankton community with
improved water transparency in May 2005–2007
matched our expectations. The euphotic depth, cal-
culated by equation provided by Reinart & Pedusaar
(2008) exceeded 2 m, reaching its highest level since
1978, suggested effect of the fish removal. Diatoms,
cryptophytes and chrysophytes dominated, restoring
some of the seasonality in phytoplankton that used to
occur in early 1960s in the lake (Pedusaar et al.,
2008). Change towards smaller species as well as
more diverse phytoplankton community have been
recorded in many restoration case studies, e.g. Lake
Trummen (Cronberg, 1982), Lake Finjasjon
(Annadotter et al., 1999) and several Finnish lakes
(Olin et al., 2006).
Contrary to our expectations, cladocerans did not
become more abundant but even decreased in 2005–
2007. One reason for the low cladoceran biomass was
probably the predation by planktivorous fish. The
problem of YOY cyprinids has been common in
many lakes after fish removal (e.g. Hansson et al.,
1998), but we did not find signs of a major invasion
of YOY cyprinids in any year. However, the densities
of YOY perch and pikeperch which were high before
the fish removal ([10,000 fish ha-1 and 19 kg ha-1
in 2003; Pedusaar et al., 2008 and unpublished data)
probably remained high since percids were not
removed and the CPUEn of perch in gillnet moni-
toring peaked in 2006. This view is supported by
results of Mills et al. (1987) from Lake Oneida,
another eutrophic lake with high density of percids.
They found that populations of Daphnia pulex could
tolerate predation by 10 kg ha-1 of YOY yellow
perch (Perca flavescens) but reproduction could not
compensate for predation when biomass of YOY was
20–40 kg ha-1. Lack of the large-sized Daphnia
galeata, which was found in the lake in the 1970s
(Pedusaar et al., 2008) but did not re-establish its
population after fish removal, also suggested that the
density of planktivorous fish was still high. Multi-
variate regression analyses showed that Daphnia had
no effect on phytoplankton biomass or Chl a. The
lake’s unchanged cladocerans community structure
may indicate that the change in food quality was not
enough. Large colonies with mucilage found in Lake
Ulemiste in summers after fish removal are regarded
inedible for zooplankton (Gliwicz & Lampert, 1990;
Rohrlack et al., 1999; Reynolds, 2007). Also the
overall food resources of zooplankton were reduced
when the biomass of phytoplankton decreased in
2006 and 2007.
The biomass of Cladocera could also be limited by
Leptodora although perch has been documented to
select Leptodora over smaller cladocerans (e.g. Lunte
& Luecke, 1990; Horppila et al., 2000). Short peaks
of Leptodora may have been possible since YOY
perch often prefer littoral habitat in mid-summer and
switch to pelagial in the latter half of summer (Urho,
1996). In June, they may also be still too small and
slow to prey on the large and evasive Leptodora. In
the end of summer, fish predation usually limits the
number of Leptodora (Liljendahl-Nurminen et al.,
2003) and we consider that lack on Leptodora in the
end of summer was caused by the high density of
pelagic YOY percids in Lake Ulemiste.
In summary, the main goal, i.e. better water
transparency for the whole vegetation period, was
not achieved in 2005–2007 although phytoplankton
biomass and Chl a decreased significantly. Decrease
in phytoplankton and especially in Chl a was primar-
ily controlled by TP availability as top-down control
was non-significant or transient. A decline in external
inputs, a heavy rainfall and the biomanipulation
coincided in time that made it difficult to attribute
the observed changes to each of them separately.
Looking to the future
There is no single, uniform cause of the poor water
quality in Lake Ulemiste and, therefore, no single
management solution. The acceptable level of external
TP loading for polymictic shallow lakes, as suggested
for successful biomanipulation (0.6 g TP m2 y-1,
Benndorf, 1990), was not exceeded in the study years
in Lake Ulemiste. However, the external loading is still
Hydrobiologia (2010) 649:95–106 103
123
exceeding often the Vollenweider’s (1976) lower
limit of critical loading (0.1–0.2 g TP m-2 y-1 for
Ulemiste). Therefore, all feasible measures to continue
reducing external loading should be regarded as a
sustainable and economically sound strategy in the
management of Lake Ulemiste, otherwise the fish
removal may have only a short-lived effect on the
quality of the lake water. Søndergaard et al. (2007)
emphasized that lake restoration should be perceived
as a management tool rather than a ‘once and for all’
solution. Although the phosphorus concentrations in
2006 and 2007 were lower than earlier, we also
consider internal loading as a potential threat to the
recovery of Lake Ulemiste and find it necessary to
study in more detail lake sediments as emphasized
earlier (Pedusaar et al., 2008). There is also a need to
make a more detailed study of both zooplankton and
phytoplankton species composition, including pico-
plankton, and the role of zooplankton predators, YOY
percids and Leptodora, so as to understand better the
functioning of Lake Ulemiste’s food web.
It seems that oligotrophication of Lake Ulemiste
leads to greater diversity in phytoplankton species
with higher contribution of colonial cyanobacteria to
total cyanobacteria biomass. This may lead to a
technical problem in the WTP because colonial
cyanobacteria clog most effectively microstrainers
that are used as a first stage in water-treatment
technology. However, an issue for debate should be
the replacement of microstrainers of the WTP by
another more efficient method.
From a management perspective, a major issue is
to determine whether the fish stock removed was
adequate or not. In eutrophic lakes and reservoirs, it
appears that the ability of large-sized daphnids to
significantly reduce phytoplankton levels can be
expected only above certain levels of fish stock
removal. Seda et al. (2000) suggested this level to be
about 70 kg ha-1 and more. As judged by the
changes of TP, the removal in 2005 was sufficient
and also the decline in fish catches themselves
suggests that the biomass of cyprinids was suffi-
ciently reduced. However, lowering the density of
YOY percids remains another challenge to be solved.
Acknowledgements We are most grateful to Tallinn Water
Ltd., Marine Systems Institute at Tallinn University of
Technology, Estonian Environment Information Centre and
Estonian Meteorological and Hydrological Institute for help
with data. The manuscript has been improved in terms of
English style thanks to Penny Mountain. A water permit for
large-scale removal of fish was issued by the Estonian Ministry
of Environment. The study was supported by Estonian Science
Foundation Grant 7656.
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