Primary Research Paper

Estimation of reference conditions for phytoplankton in a naturally

eutrophic shallow lake

Liisa Lepisto1,*, Pirkko Kauppila1, Jarkko Rapala2, Mauri Pekkarinen3, Ilkka Sammalkorpi1

& Leena Villa41Finnish Environment Institute, 140 FIN-00251, Helsinki, Finland2National Product Control Agency for Welfare and Health, 210 FIN-00531, Helsinki, Finland3Mid-Uusimaa Joint Municipal Board for Water Pollution Control, Kultasepankatu 4B, FIN-04250, Kerava, Finland4Uusimaa Regional Environment Centre, 36 FIN-00521, Helsinki, Finland(*Author for correspondence: E-mail: Liisa.lepisto@ymparisto.fi)

Received 30 September 2005; in revised form 14 January 2006; accepted 21 January 2006; published online 5 May 2006

Key words: phytoplankton, naturally eutrophic lakes, reference conditions, empirical modelling

Abstract

Classification of waters using biological quality elements and determination of the degree of deviationfrom reference levels is a key issue in the Water Framework Directive of EU. Lakes in referenceconditions with sufficient biological data are available for several boreal lake types with the exceptionof naturally eutrophic lakes. An empirical approach is one alternative for estimating the referenceconditions of such lakes. We used the water transparency of the naturally eutrophic Lake Tuusulanjarvirecorded in August in the early 1910s to estimate reference values for phytoplankton biomass andchlorophyll a concentrations. Three phytoplankton samples during August 2000–2001 corresponded tothe estimated reference values for total biomass (<5.6 mg l)1) and chlorophyll a (<28 lg l)1), as didthe simultaneous Secchi depths. The phytoplankton assemblage in these samples with 24 eutrophyindicators (17% of the total taxa number) corresponded in general the species list from the early 1900s,which as such could be regarded as reference assemblage. Furthermore, in August 2000, 3 years afterintensive fish removal a prominent decrease in cyanobacterial biomass and toxin concentration wasobserved. The costs of the measures and studies in Lake Tuusulanjarvi during 1989–2003 have beenapproximately 2.5 million euros.

Introduction

Assessment of the ecological status of surfacewaters is increasingly needed for controllingwater pollution all over world. According to theEU Water Framework Directive (WFD, Euro-pean Union, 2000), the ecological status of sur-face waters must be quantified mainly on thebasis of biological indicators. Phytoplankton isone of the biological elements known to respondto the anthropogenic impact, expressed itselfmainly as nutrient enrichment (e.g. Hutchinson,

1967). However, the composition of a phyto-plankton assemblage does not depend only onnutrients but also on biological factors (e.g.Balayla & Moss, 2004) and indirectly on mete-orological and hydrological conditions (e.g.Mattson et al., 2003). The total wet biomass,chlorophyll a concentration of phytoplanktonand indicator taxa are likely to be useful indi-cators in lakes (Lepisto et al., 2004).

The implementation of the WFD requires theestablishment of reference conditions for eachwater body type. However, there are usually few

Hydrobiologia (2006) 568:55–66 � Springer 2006DOI 10.1007/s10750-006-0032-4

if any biological data available from pristinenaturally eutrophic lakes (Lepisto et al., cit. op.).For example, the historical phytoplanktonrecords (e.g. Levander, 1900, 1914; Cleve-Euler& Huss, 1912; Jarnefelt, 1956) and even somequotients (Thunmark, 1945; Nygaard, 1949) arebased on net samples, not comparable with thepresent quantitative data. These records provideinformation of the occurrence of mainly micro-or netplankton (20–200 lm) whereas smallnanoplankton (2–20 lm) taxa are missing.Therefore, the old qualitative and even thequantitative records could only be used as astarting point (Lepisto et al., 1999) for expertjudgements.

Paleolimnological methods yield informationon the pollution history and reference conditionsboth in lakes (Tolonen et al., 1990; Rasanenet al., 2006) and in small non-tidal estuaries(Kauppila et al., 2005) and on the chronology ofenvironmental changes recorded in sediment (e.g.Battarbee, 1991; Bennion et al., 1996; Andrenet al., 1999). Empirical approaches offer analternative tool to estimate reference conditions,provided that historical data are available.In this respect, the utilization of the relation-ship between phytoplankton and Secchi depth,studied previously e.g. by Carlson (1977, 1980),Megard et al. (1980), Megard & Bergman (1989)and Sanden & Hakansson (1996), is worth con-sidering, as the monitoring of Secchi depth haslong traditions. However, the weakening of therelationships e.g. by humic substances (Lorenzen,1980; Megard et al., 1980), which are typical inmany naturally eutrophic lakes, must be takeninto account.

The aims of this study were (1) to apply anempirical approach to estimate reference valuesfor phytoplankton wet biomass and chlorophylla concentration in the naturally eutrophic LakeTuusulanjarvi using historical Secchi depth dataof the 1910s, (2) to consider the impact of re-cent conservation measures on the ecologicalstatus of the lake, focusing on phytoplanktonquantity and quality and toxin concentration ofcyanobacteria, (3) to discuss the costs of themeasures carried out, and (4) to determine pre-liminarily the present ecological status of thelake.

Material and methods

Characteristics of the study lake

The eutrophic, turbid and slightly humic LakeTuusulanjarvi is situated in the coastal lowlandarea of southern Finland. The lake is shallow andmoderately large (Table 1) and receives watermainly from three brooks. It was characterized asnaturally eutrophic by Jarnefelt (1937) in the early1900s, and is preliminarily included into this typein the characterization of Finnish lakes, due to thefertile clay soil of the drainage area. The popula-tion density around the lake was low until the 19thcentury, and started to increase in the 1950s.According to paleolimnological records (Harjula,1972, in Tolonen et al., 1990), Lake Tuusulanjarviis assumed to have developed from the oligo-trophic to the mesotrophic phase during the period1310±90, and mesotrophy turned to eutrophy in1850±14. Rapid eutrophication began around1956 due to the increased nutrient loading fromsettlements and agriculture (Jarnefelt, 1958). Thewater level of the lake has been regulated since1959 especially to reduce spring floods. It mighthave increased the growth of reed on the shores ofthe lake. There is a plan to restore the water levelof the lake towards more natural (Joensuu &Pekkarinen, 2005). Sewage discharge into thelake was discontinued in 1979 but the internalloading was still prominent (Pekkarinen, 1990).

Economical aspects of lake management

Ecological lake management planning and mea-sures, such as intensive experiments aimingat restoring sediments, water column mixing,

Table 1. Some characteristics of Lake Tuusulanjarvi

Drainage area [km2] 92

Surface area [km2] 5.95

Volume [106 m3] 19.15

Maximum depth [m] 10.0

Mean depth [m] 3.2

Theoretical retention time [d] 250

External loading of P [g m2 a)1] 0.8

Internal loading of P [g m2 a)1] 3–4*

*before restoration in the 1990s.

56

agricultural projects and initial stages of fishinvestigation were started in 1989 with the aim ofimproving water quality (Table 2). Since 1997–1998 additional measures, including prevention ofinternal loading by intensive mechanical mixing ofthe water column, and food web manipulation byselective removal of zooplanktivorous fish, werestarted (Sammalkorpi, 2000; Joensuu & Pekkari-nen, 2005; Saarijarvi & Lappalainen, 2005). Theinvestments funded by e.g. the municipalities ofJarvenpaa and Tuusula, the Ministry of theEnvironment, the Ministry of Agriculture andForestry and the EU increased to ca. 2.5 millioneuros in 1989–2003.

Phytoplankton and Secchi depth data

Lake Tuusulanjarvi is a Finnish lake with exten-sive phytoplankton data (Lepisto et al., 1999).The very first phytoplankton sampling from LakeTuusulanjarvi was carried out by netting in 1893and in 1913 by Levander (1900, 1914) and byJarnefelt (1956) in the years 1913–1917. In thelatter study the composition of the phytoplanktonassemblage was presented as the frequency of taxa.Since 1921 samples have been collected from thedeepest part of the lake and studied quantitativelyusing Kolkwitz chambers (Jarnefelt, 1937), andsince 1932 (Jarnefelt, 1958) the Utermohl-method(Utermohl, 1931, 1958). This old data was storedin the biological data set of Finnish EnvironmentInstitute (Lepisto et al., 1999). However, the oldand the present data are not fully comparable due

to methodological differences and due to difficul-ties in interpretation of the old counting unitsduring the input of data. Since 1974 the phyto-plankton and chlorophyll a samples and since 1995the toxin samples represented the 0–2 m waterlayer. Phytoplankton samples were preservedusing acidic Lugol’s solution and analysed underan inverted microscope using a Nordic variant ofthe Utermohl-method (Olrik et al., 1998). In thisstudy the data originated from August with one ortwo samplings per month. The occurrence ofphytoplankton taxa was estimated as a ratio offrequency (n of observations/n of samples) duringdifferent decades before and after the intensivemeasures in the 1990s. Cyanobacterial hepatotox-ins (microcystins) were analysed according toRapala et al. (2002).

The trophic state estimates in the early 1930swere based on the expert opinion of Jarnefelt(1937, 1956). The criteria for using total biomassto define trophic state are presented by Heinonen(1980), with biomass values for:

ultraoligotrophy <0.2 mg l)1

oligotrophy 0.21–0.5 mg l)1

oligo-mesotrophy 0.51–1.00 mg l)1

mesotrophy 1.01–2.5 mg l)1

eutrophy 2.51–10.0 mg l)1

hyper-eutrophy > 10.0 mg l)1

The first Secchi depths in 1910–1911 weremeasured using a glased faience disc with adiameter of 20 cm (Olin, 1912), which is of thesame size as the present disc used in the nationalmonitoring. The earliest total phosphorus (TP) inthe 1920s (Jarnefelt, 1937) was analysed with lessaccurate methods and instruments. Water qualitydata of Lake Tuusulanjarvi and the daily waterflow of the River Tuusulanjoki originated fromthe monitoring of the Finnish EnvironmentalAdministration in 1974–2004. The physical andchemical variables of TP, water colour and tur-bidity were taken from a depth of one meter andanalysed together with chlorophyll a according tothe Finnish standard methods described in detailby Niemi et al. (2000).

Statistical methods

Linear and multiple regression methods were usedto consider the relationships between phytoplankton

Table 2. Fundingof studies andmeasurements of the restoration

project during 1989–2003 in Lake Tuusulanjarvi

Years Measures e

1989–1992 Wide sediment investigation 36,000

1993–1997 Restoration experiments of sedi-

ments

303,000

1995–1996 Planning of loading reduction from

agriculture

58,000

1996–1997 Initial fish manipulation studies 30,000

1997–2003 Intensive fish manipulation and

studies

550,000

1998–2003 Artificial water column mixing 300,000

1999–2003 Construction of wetlands, dredging

of shores, etc.

1,150,000

1989–2003 TOTAL, e 2,427,000

57

total biomass and chlorophyll a concentrationsand Secchi depth, TP, turbidity and water colour.Regression analyses were also conducted for TPand Secchi depth. The variables were log-trans-formed to stabilize variance (Zar, 1996). Inestablishing reference conditions, the historicalconcentrations of TP, chlorophyll a and totalphytoplankton biomass were reconstructed usingthe given regression equations with Secchi depth,and the five old Secchi depth values observed inthe lake by Olin (cit. op.) in August of 1910 and1911. Phytoplankton species compositions in thosesamples, which corresponded to the estimatedreference values for biomass and chlorophyll awere then compared to the historical phytoplank-ton lists of Levander (1900, 1914) and Jarnefelt(1956).

Results and discussion

Establishing reference conditions

There is a non-linear relationship between TPand Secchi depth, and between chlorophyll aand Secchi depth in lakes (Carlson, 1977;Megard et al., 1980; Canfield et al., 1985). Fac-tors affecting these correlations include amountsof phytoplankton, the composition and agestructure of the algal assemblage, and colouredhumic substances and suspended solids (Tolstoy,1979). In Lake Tuusulanjarvi, TP and chloro-phyll a could be predicted by Secchi depth,which explained 29 and 31% of their variation(Fig. 1). Chlorophyll a was also associated withturbidity and water colour, which accounted for43 and 27% of the variation in chlorophyll a,respectively. The weak correlations betweenchlorophyll a and water transparency indicatorswere mainly due to high amounts of humicsubstances (40–140 mg Pt l)1) in the lake. Totalphytoplankton biomass had lower correlationswith Secchi depth and turbidity (r2 = 0.13 and0.09, respectively) than chlorophyll a, which wasprobably mainly due to abundance of diatoms(Lepisto et al., 2003), which overestimated thebiovolumes in relation to the cellular chloro-phyll a content. This also explains why chloro-phyll a was linked much more strongly to TP(r2 = 0.51) than was total biomass (r2 = 0.15).

The historical chlorophyll a and total phyto-plankton biomass, reconstructed by the empiricalrelationships, varied on an average between 24 and28 lg l)1 and 4.9 and 5.6 mg l)1, respectively(Table 3). The reference values for TP varied on anaverage between 94 and 100 lg l)1. These refer-ence concentrations correspond to the levels in theearly 2000s (Table 3). However, the great scatterof variables should be taken into account (Figs. 1,2), as well as the low number of historical mea-surements of Secchi depth (only five in August of1910 and 1911), which are not sufficient to showthe natural variation. Furthermore, variations inhydrological conditions affect the amounts ofleaching of nutrients and humic substances fromthe drainage area (Mattson et al., 2003), which inturn causes variation in water transparency (mea-sured by Secchi depth, turbidity, water colour) andphytoplankton quantity (Figs. 2, 3).

Changes in water quality

Only little information exists on the historicalwater quality of Lake Tuusulanjarvi before thestart of regular monitoring of water quality inthe 1960s. In the 1910s, when the lake was notyet eutrophicated, the Secchi depth in Augustvaried from 0.9 to 1.05 m (Olin, 1912), theaverage being 0.98 m (Table 3). TP concentra-tion was recorded to be 122 lg l)1, however theonly observation is from July 1921 (Jarnefelt,1937). The concentrations of chlorophyll a inAugust (ca. 60 lg l)1) and TP (ca. 150 lg l)1)between the 1970s and 1990s were extremelyhigh and the Secchi depth values were low (0.4–0.5 m), (Table 3), reflecting high disturbancescaused by human activities. In the early 2000s,water quality improved, which can be observedas an increase in Secchi depth (0.6–1.1 m) and asa decrease in the concentrations of TP (onaverage 80 lg l)1) and chlorophyll a (25 lg l)1)in August (Table 3).

Changes in phytoplankton biomass and speciescomposition

BiomassIn the early 1910s, the colour of water was re-ported to be slightly yellowish during winter and

58

(a)

(b)

(c)

Figure 1. Regression equations with confidence limits (95%) (a) for TP as a function of Secchi depth, (b) for chlorophyll a as a

function of Secchi depth and (c) for total phytoplankton biomass as a function of Secchi depth in Lake Tuusulanjarvi.

59

greyish in spring and autumn. During summer thewater colouring varied from yellowish to olivebrown due to the abundant phytoplankton. The‘colouring’ became visible in the early 1920s andcyanobacterial blooms were observed in 1926(Olin, 1912; Jarnefelt, 1921, 1937). Using generalregression equations, the TP of 122 lg l)1 in 1921would have resulted in a phytoplankton biomassof at least 6–7 mg l)1 (Figs. 3, 4). In fact, the very

low biomasses of 1.0 mg l)1 (Table 3) were obvi-ously underestimations due to the uncertainty ininterpretation of the old counting results. Thebiomass in August was highest, on average21 mg l)1, in the 1970s but decreased to 14 mg l)1

in the 1980s as a consequence of the sewagediversion in 1979 (Pekkarinen, 1990; Lepisto et al.,1999). The biomass has decreased further to5 mg l)1 on average since 1998 (Table 3), due to

Table 3. Average phytoplankton biomass, chlorophyll a concentration (chl a), Secchi depth, total phosphorus (TP) values, and

cyanobacterial hepatotoxin (microcystin) concentrations in Lake Tuusulanjarvi measured in August in 1910–2003

Years Biomass (mg l)1) Taxa (n) Chl a (lg l)1) Secchi (m) TP (lg l)1) Microcystin (lg l)1)

1910–11 (4.9–5.6) (24–28) 1.0 (94–100)

1913–15 45

1921–32 (6.0–7.0) 1.0 80 122

1946 (>7.0) 1.0

1974–1979 22.0 61 0.5 149

1980–1989 18.0 69 0.4 138

1990–1997 13.0 79 0.4 142 3.48*

1998–2003 5.1 37 0.7 101 1.16

Samples in 2000–2001 corresponding the estimated reference values for total phytoplankton biomass (<5.6 mg l)1) and chlorophyll

a (<28 lg l)1).

8.8.2000 4.1 91 24 1.1 79 0.28

22.8.2000 4.6 79 33 0.9 69 0.52

21.8.2001 2.8 89 19 1.0 88 0.72

The values measured in 2000–2001 are compared with the background phytoplankton biomass and chlorophyll a values (indicated in

brackets), which were estimated using a linear regression model. n=number of samples or taxa (*in 1995–1997).

Figure 2. Variations of Secchi depth (m), Chlorophyll a (lg l)1) and Colour (mg Pt l)1) in Lake Tuusulanjarvi and variation of water

flow (m s)1) in the River Tuusulanjoki in August 1975–2004. Note, that this figure includes only the years when the results

of measurements in all these variables were available.

60

the intensive management efforts (Joensuu & Pe-kkarinen, 2005), (Table 2).

Reference concentrations of total biomass andchlorophyll a were estimated as 5.6 mg l)1 and28 lg l)1, respectively, using the regression model.Three phytoplankton samples (total biomass andchlorophyll a concentration) in August 2000–2001were below the reconstructed historical values(Fig. 4, Table 3). Simultaneously Secchi depthreached its historical reference value. Actually thesummer of 2000 showed the first signs of recovery,not only as a decrease of total phytoplankton butalso as a decrease of cyanobacterial biomass andhepatotoxin concentration (Table 3) measured

from the lake water (Lepisto et al., 2005). Thechlorophyll a concentration in August did not re-flect unambiguously the different phases of lakeloading, but since 1998 it has decreased to37 lg l)1, on average (Table 3).

Since mid-August 2002 the Secchi depthremained low (Fig. 3), obviously as a conse-quence of the reduction of the fish removal since2001–2002, which in turn was assumed to be themain causative agent for the observed increase oftotal phytoplankton and cyanobacterial biomass(Lepisto et al., 2005). This is in accordance withexperimental manipulations in lakes, which showthat intense planktivorous fish predation can be

Figure 3. Variation of total biomass, biomass of cyanobacteria and the Secchi depth in Lake Tuusulanjarvi in August 1968–2003. Note

that each grey square connected with a black dot represents one sampling occasion.

Figure 4. The total phytoplankton biomass vs. concentrations of total phosphorus in Lake Tuusulanjarvi in August 1968–2003.

Samples taken after the start of intensive management measures in 1998 are indicated as black dots. Three samples in 2000–2001

corresponding to the estimated total phytoplankton biomass (<5.6 mg l)1) are indicated with arrows. The estimated (see Fig. 2c)

average biomass (5.6 mg l)1) and the upper limit of the estimated biomass (10 mg l)1) are indicated by lines.

61

associated with increased chlorophyll a and re-duced water clarity (Mazumder et al., 1990).However, in August 2002, the minimum chloro-phyll a value (17 lg l)1) coincided with a ratherhigh biomass value (6.4 mg l)1), which exceededthe estimated reference biomass (Fig. 4). At thesame time the toxin concentration (1.13 lg l)1)was elevated compared to the three samples in2000–2001 (Table 3). It must be pointed out,that total biomass and chlorophyll a are differentkinds of indicators that are not necessarilycommensurate. Thus, the analyses of phyto-plankton should include not only total biomassbut also species composition, which enlighten theeutrophication dynamics.

Species compositionIn the early 1900s altogether 38 phytoplanktontaxa were observed in the net samples. A total of22 taxa (58%) were eutrophy-indicating, accord-ing to the criterion of e.g. Hutchinson (1967),Heinonen (1980) and Brettum (1989). ExcludingPlanktothrix (Jarnefelt, 1958), the taxa of theyears 1913–1946 represent the typical species ofnaturally eutrophic lakes (Fig. 5). ChrysomonadsDinobryon bavaricum Imhof and D. divergensImhof, and the moderately robust diatom Tabel-laria fenestrata (Lyng.) Kutzing disappeared fromthe phytoplankton community during the 1920sand 1930s (Jarnefelt, 1937). These algae were onlysporadically observed during each study period(Fig. 5). In fact, Tabellaria favours mesotrophiclakes in Finland (Lepisto, 1999). Dinobryon andTabellaria were succeeded by the cyanobacteriaAnabaena and Aphanizomenon and later byPlanktothrix and Microcystis (Jarnefelt, 1956).The increase of the N2-non-fixing Planktothrixreflected the prevailing high nitrogen concentra-tions (Varis, 1990). Ten taxa (Fig. 5) have beenrecorded frequently during the study period ofone century: the cyanobacteria Microcystis aeru-ginosa Kutzing, Anabaena flos-aquae Brebisson,A. spiroides Klebahn and Aphanizomenon spp.,the diatoms Aulacoseira granulata (Ehr.) Simon-sen, A. italica (Ehr.) Simonsen and Asterionellaformosa Hassall and the green algae Coelastrummicroporum Nageli, Dictyosphaerium pulchellumWood and Pediastrum duplex Meyen.

In the 1990s the improvement of the lakewas reflected as increase of cryptomonads and

diatoms and as decrease of cyanobacteria(Lepisto et al., 2003). According to Van DerVeer et al. (1995), the competition efficiency ofcyanobacteria, mainly Microcystis, compared tothe other algal groups is affected by the artificialmixing of the water column. Microcystis viridis(A. Braun) Lemmermann was present already in1910–1915 (Levander, 1910, 1914; Jarnefelt,1956), appeared again with low frequency in the1970s and has increased especially since 1998.This increased frequency of M. viridis might havebeen, however, a consequence of the water mixingand the rather warm summer weather since thelate 1990s (Lepisto et al., 2003). M. wesenbergii(Kom.) Starmach was not observed earlier than1998 (Fig. 5). Cyanobacterial toxin concentra-tions have correlated strongly with the biomassof the mixed populations of M. viridis andM. wesenbergii (Lahti et al., 1997; Lepisto et al.,2005).

The diatom Rhizosolenia longiseta Zachariaswas observed during the eutrophication periodsof the 1960s and 1970s, whereas the fragileRhizosolenia eriensis H.L. Smith was observedonly in the turn of the century (Levander, 1900,1914; Jarnefelt, 1956). Thereafter it has been ob-served only once, in September 2001. This diatomis known to decrease during the increasingeutrophication (Davis, 1964). ChrysomonadsDinobryon bavaricum and D. divergens wereabsent during the highest nutrient load periodsand D. suecicum Lemmermann has been observedonly during 1998–1999. An interesting featurewas the decrease of large-celled and robustAulacoseira granulata. According to Stoermeret al. (1985), this phenomenon is a consequenceof silica depletion during high nutrient loading.The large celled taxon was succeeded by thenarrow form A. granulata v. angustissima(O. Mull.) Simonsen. Since 1998 this coarsediatom has been more frequent (Fig. 5). Several‘new’ taxa were identified due to the improvedoptics, like the diatom Skeletonema potamos(Weber) Hasle (Turkia & Lepisto, 1997) but alsodue to the taxonomic resolution especially ofthe cyanobacteria. In the three reference samplesthe total number of taxa was 138, includingapproximately 24 (17%) eutrophy-indicatingspecies (Heinonen, 1980), which could be con-sidered as typical for naturally eutrophic lakes

62

(Lepisto et al., 2004). This proportion was clearlylower than in the old net samples. The onlyobservation of an oligotrophy-indicating species,the chrysomonad Dinobryon bavaricum, whichwas rather common in the early 1900s (Jarnefelt,1958), (Fig. 5), was from July 2001.

Ecological and economical evaluation of lakemanagement

Palaeolimnological analyses of sediment diatomcommunity structure (Rasanen et al., 2005) sug-gest that reference conditions in the naturally

eutrophic lakes of southern Finland, such asLake Tuusulanjarvi, existed before the 1300s. InNordic countries, however, natural conditionsare assumed to be existed before industrializationin the mid-1800s. In the late 1800s most of theFinnish lakes became also enriched with nutri-ents as a consequence of burn-beating for culti-vation. The elevated summertime concentrationof TP (122 lg l)1) in the 1920s (Jarnefelt, 1937)was, however, lower than the level during thehighest loading period in the 1970s (Table 3). Bycontrast, the present TP concentrations are ca.100 lg l)2.

Figure 5. The most important taxa during different periods in August 1913–2003 in Lake Tuusulanjarvi. The boxes represent

assemblages of species whose names are listed below. Abbreviations to species: Coel kue = Coelosphaerium kuetzingianum, Micr

flo = Microcystis flos-aquae, Micr vir = Microcystis viridis, Woro nae = Woronichinia naegeliana, Dino bav = Dinobryon bavaricum,

Dino div = D. divergens, Mall aca = Mallomonas acaroids, Aula isl = Aulacoseira islandica, Frag cap = Fragilaria capucina, Tabe

fen/flo = Tabellaria fenestrata (T. flocculosa), Pedi bor = Pediatrum boryanum, Eudo ele = Eudorina elegans, Chro limn = Chroo-

coccus limneticus, Snow lac = Snowella lacustris, Plan aga = Planktothrix agardhii, Acan zac = Acanthoceras zachariasii, Aula gra v

ang = A. granulata v. angustissima, Aula ita v ten = A. italica v. tenuissima, Rhiz lon = Rhizosolenia longiseta, Micr

wes = Microcystis wesenbergii, Skel pot = Skeletonema potamos. The average biomass of each period is shown by an arrow.

63

Based on the results of the present study, theamounts of TP and phytoplankton are nowadaysclose to those in the 1920s and the empiricallyestimated values. In addition to the biomass closeto approximately 5 mg l)1 or chlorophyll a con-centration close to 27 lg l)1, the species compo-sition also reflected improvement of the lake.The occurrence, although occasional, of thechrysomonad genus Dinobryon and the diatomRhizosolenia eriensis could be considered as asign of amelioration of the ecological status ofthe lake. Furthermore, the size variation of dia-toms reflected indirectly the heavy pollutionand the recovery (Willen, 1987, 1992) of LakeTuusulanjarvi due to the many restoration activi-ties in the basin since 1989. However, speciesindicating eutrophy have been observed through-out the past hundred years, and they belong to thetypical taxa in such a naturally eutrophic lake.

Intensive measures, such as mixing of thewater column, and food web manipulation car-ried out since 1998 (Sammalkorpi, 2000; Rasket al., 2005), were successful in the short term(Lepisto et al., 2003, 2005). For managementpurposes, however, the critical question can beposed whether it is acceptable to apply the ref-erence conditions of Lake Tuusulanjarvi pre-vailing in the early 1900s. According to theGuidance document CIS (2003), ‘in controllinganthropogenic pressures it is unrealistic to basereference conditions upon historic landscapesthat no longer exist in modern Europe’. It wouldrequire strong water protection activities in orderto further improve the status as a continuationof the effective restoration managements alreadymade. Furthermore, the practical difficulties ofdetermining reference conditions before the early1900s should be borne in mind. As there are nohistorical data for comparison from this period,additional information could be obtained bypaleolimnological methods.

Concluding remarks

The estimated reference values of phytoplanktonbiomass, chlorophyll a and TP in this studyare approximate and include thus uncertainty.Weather conditions together with many internaland external processes in the water in this shallow

and eutrophic lake affect the variation in nutrientsand phytoplankton, especially cyanobacteria andeven the cyanobacterial toxin concentrations.However, the results of the present study showthat the amounts of TP and phytoplankton arenowadays close to those in the 1920s and theempirically estimated natural values. Furthermonitoring of the lake will hopefully reflect anincreasing stability in the biomass values eventhough inter-annual variation, sometimes of aconsiderable range, are to be expected in shalloweutrophic waters. Furthermore, changes in thespecies composition or size structure reflect di-rectly or indirectly improvement of the lake. Asreference taxa for naturally eutrophic lakes couldbe regarded the mainly eutrophy-indicating taxaobserved in 1913–1946. In the three referencesamples the proportion of eutrophy indicators wasdecreased to 17%.

The economical investments of restoration ofLake Tuusulanjarvi have been some millions ofEuros. The most costly measures were the inten-sive construction of wetlands, shoreline manage-ment and fish removal. Strong water protectionactivities are still required in the future to improvethe status as a continuation to the effective resto-ration measures already implemented. Regardingnaturally eutrophic lakes with a long anthropo-genic history, it is unrealistic to set reference con-ditions before the 1800s, when these lakes were stillmore or less pristine due to the low human pres-sure with only minor ecological effects.

Acknowledgements

The authors wish to thank Reija Jokipii and MaijaNiemela for the phytoplankton analysis, MichaelBailey for revising the English of the manuscriptand Erika Varkonyi and Ritva Koskinen forpreparing the figures.

References

Andren, E., G. Shimmield & T. Brand, 1999. Environmental

changes of the last three centuries indicated by siliceous

microfossil records from the South-Western Baltic Sea.

Holocena 9: 25–38.

Balayla, D. J. & B. Moss, 2004. Relative importance of grazing

on algae by plant-associated and open-water microcrustacea

(Cladocera). Archiv fur Hydrobiologie 161: 199–224.

64

Battarbee, R. W., 1991. Recent palaeolimnology and diatom-

based environmental reconstruction. In Shane, L. C. & E. J.

Cushing (eds), Quaternary Landscapes. Belhaven Press,

London,: 129–174.

Bennion, K. D., S. Juggins & N. J. Anderson, 1996. Predicting

epilimnetic phosphorus concentrations using an improved

diatom-based transfer function and its application to lake

eutrophication management. Environmental Science &

Technology 30: 2004–2007.

Brettum, P., 1989. Alger som indikator pa vannkvalitet i norske

innsjøer. Planteplankton. Niva-Rapport 0-86116, 111 pp.

[Algae as indicators of water quality in Norwegian lakes.

Phytoplankton].

Canfield, D. E., Jr., S. B. Linda & L. M. Hodgson, 1985.

Chlorophyll – biomass – nutrient relationships for natural

assemblages of Florida phytoplankton. Water Resources

Bulletin WARBAQ 21(3): 381–391.

Carlson, R. E., 1977. A trophic state index for lakes. Limnology

and Oceanography 22: 361–368.

Carlson, R. E., 1980. More complications in the chlorophyll-

Secchi disk relationship. Limnology and Oceanography 25:

379–382.

Cleve-Euler, A. & H. Huss, 1912. Vattnet i sjoar och vattendrag

inom Stockholm och dess omgivningar. II. Plankton-

undersokningar. [Water in lakes and watercourses in

Stockholm and its surroundings. II. Plankton studies].

CIS, 2003. Transitional and coastal waters – Typology, refer-

ence conditions and classification systems. Common imple-

mentation strategy for the Water Framework Directive

(2000/60/EC). Guidance document No 5. European Com-

munities, 2003.

Davis, C. C., 1964. Evidence for the eutrophication of Lake

Erie from phytoplankton records. Limnology and Ocean-

ography 3: 275–283.

European Union, 2000. Establishing a framework for Com-

munity action in the field of water policy. Directive of the

European Parliament and of the Council 2000/60/EC. Offi-

cial Journal of the European Communities, L327, 72 pp.

Harjula, H., 1972. Hiidenveden ja Tuusulanjarven rehevoity-

misen kehitys pohjasedimenttien valossa. University of Hel-

sinki, department of limnology, 109 pp. [The development of

eutrophication in lakes Hiidenvesi and Tuusulanjarvi as re-

corded from bottom sediments], unpublished Lic. Phil. thesis.

Heinonen, P., 1980. Quantity and composition of phytoplank-

ton in Finnish inland waters. Publications of the Water

Research Institute, Helsinki, 37, 91 pp.

Hutchinson, G. E., 1967. A treatise on Limnology, II. John

Wiley & Sons, Inc, New York, 1115 pp.

Joensuu, I. & M. Pekkarinen, 2005. Cultural eutrophication,

restoration and management of Lake Tuusulanjarvi. Ver-

handlungen Internationale Vereinigung fur theoretische und

angewandte Limnologie 29 (in press).

Jarnefelt, H., 1921. Fische und ihre Nahrung. Acta Societatis

pro Fauna et Flora Fennica 52: 1–60.

Jarnefelt, H., 1937. Ein kleiner Beitrag zur Limnologie des

Tuusulanjarvi.Acta Societatis proFauna et FloraFennica 60:

502–515.

Jarnefelt, H., 1956. Materialen zur Hydrobiologie des Sees

Tuusulanjarvi. Acta Societatis pro Fauna et Flora Fennica

71: 1–38.

Jarnefelt, H., 1958. Weiterer Beitrag zur Limnologie des

Tuusulanjarvi. Acta Societatis pro Fauna et Flora Fennica

74: 1–17.

Kauppila, P., K. Weckstrom, S. Vaalgamaa, A. Korhola, H.

Pitkanen, N. Reuss & S. Drew, 2005. Tracing pollution and

recovery using sediments in an urban estuary, northern

Baltic Sea: are we far from ecological reference conditions.

Marine Ecology Progress Series 290: 35–53.

Lahti, K., J. Rapala, M. Fardig, M. Niemela & K. Sivonen,

1997. Persistence of cyanobacterial hepatotoxin, microcy-

stin-LR in particulate matter and dissolved in lake water.

Water Research 31: 1005–1012.

Lepisto, L., 1999. Phytoplankton assemblages reflecting the

ecological status of lakes in Finland. Monographs of the

Boreal Environment Research 16: 1–43.

Lepisto, L., A. -L. Holopainen & H. Vuoristo, 2004. Type-

specific and indicator taxa of phytoplankton as a quality

criterion for assessing the ecological status of Finnish boreal

lakes. Limnologica 34: 236–248.

Lepisto, L., K. Lahti, J. Rapala, L. Villa & I. Sammalkorpi,

2005. The effects of fish removal on cyanobacteria and their

toxicity in Lake Tuusulanjarvi. Verhandlungen Internatio-

nale Vereinigung fur theoretische und angewandte Limnol-

ogie 29: 473–477.

Lepisto, L., A. Raike & O. -P. Pietilainen, 1999. Long-term

changes of phytoplankton in a eutrophicated boreal

lake during the past 100 years (1893–1998). Archiv fur

Hydrobiologie, Supplement 129, Algological Studies 94:

223–244.

Lepisto, L., I. Sammalkorpi, R. Jokipii & M. Niemela, 2003.

Effectes of destratification and fish removal on the genus

Microcystis in a shallow hypertrophic lake. Archiv fur Hy-

drobiologie, Supplement 148, Algological Studies 109: 375–

386.

Levander, K. M., 1900. Zur Kentniss der Fauna und Flora

finnischer Binnenseen. Acta Societatis pro Fauna et Flora

Fennica 19: 1–55.

Levander, K. M., 1914. Foreteckningar ofver planktonter i

Tusbutrask. Meddelanden af Societas pro Fauna et Flora

Fennica 40: 49–53. [Description of phytoplankton in Lake

Tuusulanjarvi].

Lorenzen, M. W., 1980. Use of chlorophyll-Secchi disk rela-

tionships. Limnology and Oceanography 25: 371–372.

Mazumder, A., W. D. Taylor, D. J. McQueen, D. R. S. Lean &

N. R. Lafontaine, 1990. Comparison of lakes and lake

enclosures with contrasting abundances of planktivorous

fish. Journal of Plankton Research 12: 109–124.

Mattson, T., L. Finer, P. Kortelainen & T. Sallantaus, 2003.

Brook water quality and background leaching from un-

managed forested catchments in Finland. Water, Air and

Soil Pollution 147: 275–297.

Megard, R. O., J. C. Settle, H. A. Boyer & W. S. Combs Jr,

1980. Light, Secchi discs, and trophic states. Limnology and

Oceanography 25: 373–377.

65

Megard, R. O. & T. Bergman, 1989. Effects of algae on the

Secchi transparency of the southeastern Mediterranean Sea.

Limnology and Oceanography 34: 1640–1655.

Niemi, J., P. Heinonen, S. Mitikka, H. Vuoristo, O. -P. Pie-

tilainen, M. Puupponen & E. Ronka, 2000. The Finnish Eu-

rowaternet: the European agencies monitoring network for

Finnish inland waters. The Finnish Environment 445: 1–62.

Nygaard, G., 1949. Hydrobiological studies on some Danish

ponds and lakes. II. The quotient hypothesis and some new

or little known phytoplankton organisms. Det Kongelige

Danske Videnskabernes Selskabs publikationer Biologiske

Skrifter 7: 1–293.

Olin, V. V., 1912. Bidrag till Tusbytrasks morfometri och optik.

Mimeograph, University of Helsinki, dep. geography, 66

pp. [Survey of the morphometry and optic of Lake

Tuusulanjarvi].

Olrik, K., P. Blomqvist, P. Brettum, G. Cronberg & P. Elo-

ranta, 1998: Methods for quantitative assessment of phyto-

plankton in freshwaters, part I. Naturvardsverket,

Stockholm, 86 pp.

Pekkarinen, M., 1990. Comprehensive survey of the hypertro-

phic Lake Tuusulanjarvi – nutrient loading, water quality

and prospects of restoration. Aqua Fennica 20: 13–25.

Rapala, J., K. Erkomaa, J. Kukkonen, K. Sivonen & K. Lahti,

2002. Detection of microcystins with protein phosphatase

inhibition assay. Comparison of methods. Analytica Chi-

mica Acta 466: 213–231.

Rask, M., J. Ruuhijarvi, M. Olin, A. Lehtovaara, S. Vesala & I.

Sammalkorpi, 2005. Responses of zooplankton and fish to

restoration in a eutrophic lake, Tuusulanjarvi, in southern

Finland. Verhandlungen Internationale Vereinigung fur

theoretische und angewandte Limnologie 29: 545–549.

Rasanen, J., T. Kauppila & V.-P. Salonen, 2006. Sediment-

based investigation of naturally or historically eutrophic

lakes – implications for lake management. Accepted in

Journal of Environmental Management .

Saarijarvi, E. & K. M. Lappalainen, 2005. Regulation of

stratification as a tool for improving hypolimnetic oxy-

gen state. Verhandlungen Internationale Vereinigung fur

theoretische und angewandte Limnologie 29: 1037–1042.

Sammalkorpi, I., 2000. The role of fish behaviour in biomanip-

ulation of a hypertrophic lake. Verhandlungen Internationale

Vereinigung fur theoretische und angewandte Limnologie 27:

1464–1472.

Sanden, P. & B. Hakansson, 1996. Long-term trends in Secchi

depth in the Baltic Sea. Limnology and Oceanography 41:

346–351.

Stoermer, E. F., J. Wolin, C. Schelske & D. Conley, 1985.

Variations in Melosira islandica valve morphology in Lake

Ontario sediments related to eutrophication and silica

depletion. Limnology and Oceanography 30: 414–418.

Thunmark, S., 1945. Zur Zoologie des Susswasserplanktons.

Eine methodologisch-okologische Studie. Folia Limnologica

Scandinavica 3: 1–66.

Tolonen, K., V. Ilmavirta, H. Hartikainen & J. Suksi, 1990.

Paleolimnological investigation of the eutrophication history

of lake Tuusulanjarvi, Southern Finland. Aqua Fennica 20:

27–41.

Tolstoy, A., 1979. Chlorophyll a in relation to phytoplankton

volume in some Swedish lakes. Archiv fur Hydrobiologie 85:

133–151.

Turkia, J. & L. Lepisto, 1997. Skeletonema potamos (Weber)

Hasle, a diatom newly found in Finnish lakes. Archiv fur

Hydrobiologie, Supplement 120, Algological Studies 86:

39–49.

Utermohl, H., 1931. Neu Wege in der quantitativen Erfassung

des Planktons. Verhandlungen Internationale Vereinigung

fur theoretische und angewandte Limnologie 5: 567–596.

Utermohl, H., 1958. Zur Vervollkommnung der quantitativen

Phytoplankton-Methodik. Mitteilungen Internationale Ve-

reinigung fur theoretische und angewandte Limnologie 9:

1–38.

Varis, O., 1990. Development of phytoplankton community in

a restored eutrophic lake – A multivariate analysis. Ver-

handlungen Internationale Vereinigung fur theoretische und

angewandte Limnologie 24: 693–697.

Van Der Veer, B., J. Koedood & P. M. Visser, 1995. Artificial

mixing: a therapy measure combating cyanobacteria in Lake

Nieuwe Meer. Water Science & Technology 8: 245–248.

Willen, E., 1987. Phytoplankton and reversed eutrophication in

Lake Malaren, Central Sweden, 1965–1983. British Phyco-

logical Journal 22: 193–208.

Willen, E., 1992. Long-term changes in the phytoplankton of

large lakes in response to changes in nutrient loading. Nordic

Journal of Botany 12: 577–587.

Zar, J. H., 1996. Biostatistical Analysis. Englewood Cliffs,

Prentice-Hall, 662 pp.

66