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

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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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