Limnologica34,236-248 (2004) ELSEVIER http://www.elsevier.de/limno HMNOLOGICA

Type-specific and indicator taxa of phytoplankton as a quality criterion for assessing the ecological status of Finnish boreal lakes

Liisa Lepist6 I,*, Anna-Liisa Holopainen 2, Heidi Vuoristo 1

Finnish Environment Institute, Helsinki, Finland 2 Karelian Research Institute, University of Joensuu and North Karelian Environment Centre, Joensuu, Finland

Received: June 16, 2004 • Accepted:August 9, 2004

Abstract

Key issues in the implementation of the Water Framework Directive are classification of lakes using biological quality parameters and type-specific reference conditions. This work is one of three studies considering different metrics of phytoplankton in the classification of ecological status. Phytoplankton was studied in a total of 55 Finnish boreal lakes, including 32 reference lakes. We tested the suitability of taxonomic composition and abundance of phytoplankton groups for biological classification. We also preliminarily determined the type-specific taxa for the studied lakes. The type-specific taxa for reference conditions are coincidently the indicator species/taxa for high ecological status. Interestingly, some taxa type-specific for impacted oligo-humic lakes proved to be the type-specific taxa for humic reference lakes. The pressure of human impact was observed not only as increase of biomass but also as changes in the species composition. The phytoplankton composition indicated the ecological status of impacted lakes moderately well. There was some variation in the indica- tions given by different algal groups, probably due to the preliminary class boundaries used. However, the preliminary combination of indicative parameters to estimate the ecological status of the studied impacted lakes was in general in accordance with earlier classification of water quality in Finnish lakes.

Key words: Phytoplankton composition - type-specific taxa - indicator taxa - indicator pa- rameters - Water Framework Directive - ecological status

Introduction structure (taxa, abundances and biomass) and function (response to the environmental conditions) of phyto- Phytoplankton is known to react sensitively to differ- plankton is important when assessing the links between ences in catchment-derived chemical characteristics phytoplankton and the environment. (RosEN 1981; ARVOLAet al. 1999). Indicator species for Diverse phytoplankton assemblages occur in natural different nutritional levels have been presented for olig- waters spatially and temporally (HUTCHINSON 1967; otrophic waters as well as for waters with increased an- HOLOPAINEN et al. 2003). This is based on the abundance thropogenic pollution (J~RNEFELT 1952; BRETTUM of a species as "inoculum" or on the ability of a species 1989). WmLgN (2000) pointed out that knowledge of the to increase at a greater rate than its competitors

*Corresponding author: Liisa Lepist6, Finnish Environment Institute, RO. Box 140, FIN-O0251 Helsinki, Finland; Phone: +358 9 40300312, Fax: +358 9 40300390; e-mail address: [email protected]

0075-9511/04/34/03-236 $ 30.00/0 Limnologica (2004) 34,236-248 Type-specific and indicator taxa of phytoplankton 237

(REYNOLDS 1986). Phytoplankton assemblages may be Phytoplankton data designated by the name of one or more dominant species. However, according to HUTCHINSON (1967) Phytoplankton samples were collected from a depth of enumeration of rare, characteristic species can in some 0-2 metres, and preserved using acidic Lugol's solution. cases provide more information about the lake. When Simultaneously, samples for water chemistry were taken looking for type-specific taxa for different lake types, it from a depth of one metre. Phytoplankton biomass was is important to distinguish the indifferent taxa occurring estimated by microscopy using a Nordic variant of the in all lakes from the type-specific taxa, i.e. taxa observed Uterm6hl technique (UTE~MOHL 1958; OLRII~ et al. only in each lake type of reference or impacted condi- 1998), and phase-contrast illumination at x200 and tions. x 800-1200 magnifications by a trained group of investi- The taxonomic composition and abundance of phyto- gators. Cell counts were converted to biovolumes using plankton is one of the biological metrics in the norma- the cell volumes of the phytoplankton database of the tive definitions of ecological status classification in the Finnish Environment Institute. The analysis produced a Water Framework Directive, Annex 1.2 (European list with biovolumes of observed species/taxa, the Union 2000). biomass of different algal groups, and the total phyto- The aim of this study was to consider (i) whether the plankton biomass given as fresh weight, mg 1-1 (Tables 1 type-specific taxa for different ecological status of lakes, and 2). Chemical water quality was analysed according and (ii) the indicator taxa for high ecological status, i.e. to standard methods (NmMI et al. 2000). Of these phos- reference conditions, assumed by the Water Framework phorus and nitrogen concentrations, water colour, pH Directive can be determined. We also discuss (iii) how and chlorophyll a concentrations were used in this study anthropogenic impact manifested as eutrophication is (Tables 1 and 2). reflected as changes in phytoplankton assemblages and in type-specific taxa composition and (iv) how the per- Statistical analysis centage and the biomass of some algal groups determine the ecological status of the studied impacted lakes. To discriminate the reference lakes the correlations be- tween phytoplankton assemblages using the algal taxa biomass and water quality were examined by dedrended correspondence analysis (DCA) using the CANOCO Material and Methods computer program (TEe BRAAK 1987, 1990). Cumula- tive distribution function was used when setting the Characteristics of the study lakes class boundary between high and good ecological status We selected a total of 55 lakes for our study. These lakes for the type-specific indicator species in the studied lake belong to the national water-quality monitoring net- groups. work, and were sampled for phytoplankton and water chemistry in July 2002. The study lakes were mostly lo- Determination of type-specific and indicator taxa, cated in southern Finland, with some lakes in eastern and ecological status of impacted lakes and northern parts of the country (Fig. 1). The estimated mean depth of the lakes varied from 0.5 to 21 metres. The Water Framework Directive (European Union The area of the lakes (or main basins) varied from 0.04 2000) assumes nomination of type-specific taxa. Phyto- to 1040 km 2. plankton species/taxa were discriminated with the DCA- The complete set of lakes was divided in two parts: analysis. Taxa, which were observed only in a particular reference lakes with no or only very minor anthro- reference lake type, were nominated as type-specific pogenic alterations, and impacted lakes. In this study the taxa. Furthermore, cumulative distribution function was term "impacted" is used to refer to non-reference lakes used to select the 90 th percentile as a class boundary for reaching at best the ecological status of good. The divi- indicator species/taxa between high and good ecological sion was based mainly on expert judgment in the Finnish status. Furthermore, taxa, which were observed only in Environment Institute. A total of 32 reference lakes were impacted lakes of a particular type were nominated type- selected and phytoplankton assemblages in lake groups specific for impacted lakes. (Fig. 2) were compared to those of 23 impacted lakes The ecological quality ratio EQR (median value in the with typology characteristics corresponding rather reference lake group/observed value in impacted lakes) closely to those of the reference lake groups. of the biomass and the percentage of cyanobacteria and In this paper we use the appellations: diatoms were applied for preliminary determination of - "oligo-humic" for lakes with water colour < 60 mg 1-1 Pt; the ecological status of 23 impacted oligo-humic and - "humic" for lakes with water colour 60-120 mg 1-1 Pt; humic lakes. The ecological status was assessed on the - "dystrophic" for lakes with water colour > 120 mg 1-1 Pt. basis of the scale presented in the Refcond Guidance

Limnologica (2004) 34,236-248 238 L. Lepist6 et al.

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Fig. 1. The observation sites in July 2002. Reference lakes (grey dots): 1 = Haukkajhrvi; 2 = Hormajhrvi; 3 = Pihlajavesi; 4 = An~tti; 5 = Unarinj~rvi; 6 = Valkea-Kotinen; 7 = Karjalan Pyh~j~rvi; 8 = Iso-Hietaj~irvi; 9 = Lika-Py6ree; 10 = Inarij~rvi; 11 = Iso-L6yt~ne; 12 -- Iso-Araj~rvi; 13 = Iso-Hanhij~rvi; 14 = Iso-Haukivesi; 15 = Iso-Helvetinj~rvi; 16 = Kallioj~rvi; 17 = Kattilaj~rvi; 18 = Kukkia; 19 = Kuolimo; 20 = Pielinen; 21 = Punelia; 22 = Puuj~rvi; 23 = P~ij~nne 78; 24 = Saimaa, Ilkonselk~; 25 = Saimaa, Riutanselk~; 26 = Siikaj~rvi; 27 = Sh~iksj~rvi; 28 = Vehkaj~rvi; 29 = Vuohij~rvi; 30 = Mallasvesi, 31 = Yli-Kitka; 32 = N~sij~rvi. Impacted lakes (black dots): 33 = Iso-Roine; 34 = Roine; 35 = Katumaj~rvi; 36 = Kernaalanj~rvi; 37 = Tarjannevesi; 38 = Kyr6sj~rvi; 39 = Lappaj~irvi; 40 = P~ij~nne 71; 41 = L~ngelm~ivesi; 42 = Haukk@irvi; 43 = M~yh~j~rvi; 44 = Ouluj~rvi; 45 = Houhaj~rvi; 46 = P-Kallavesi; 47 = Porttipahta; 48 = Vanajanselkh; 49 = Vanaja; 50 = Vesij~irvi; 51 = Pyh~ij~rvi 93; 52 = Pyh~j~rvi, Sorvanselk~; 53 = P~j~irvi; 54 = Rehtij~rvi; 55 = Toisvesi.

Limnologica (2004) 34,236-248 Type-specific and indicator taxa of phytoplankt0n 239

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Limnologica (2004) 34,236-248 240 L. Lepist6 et al.

(2003), applying EQR-ratios of 0.8 for high, 0.6 for blages in the DCA ordination analysis. The main part of good and 0.4 for moderate as boundaries between class- the study reference lakes, i.e. the oligo-humic lakes with es. The primary definition of ecological status was com- water colour ~ 60 mg 1-1 Pt, were grouped together. pared to the general water quality classification of However, mainly large lakes were clustered at the upper Finnish lakes. The classification into excellent, good, end of the axis 2, and oligo-humic moderately large satisfactory, passable and poor is based on physico- lakes were clustered at the opposite end. One small lake chemical water quality (VUORISTO 1998). (lake No. 27) with a low water colour of 8 mg 1-1 Pt was an outlier (Tables 1 and 2, Fig. 2). Humic lakes formed a separate group on the axis 1. Results Furthermore, two dystrophic lakes and two acidic (pH 5.3-5.5) small lakes, one humic and one dystrophic There was a wide variation in total phytoplankton (100-160 mg 1-t Pt) were grouped at opposite ends of the biomass, concentrations of nutrients and water colour in axis 1 (Fig. 2). the whole dataset (Tables 1 and 2). Phytoplankton biomass in the studied 55 lakes varied from 0.12 mg 1-1 , measured in the reference Lake Iso-Hietajfirvi (lake No. Algal groups, type-specific and indicator taxa 8), to 5.71 mg 1-1 in the impacted Lake Houhaj/irvi (lake in the study lakes No. 45). • Oligo-humic lakes Groups of reference lakes In oligo-humic large reference lakes (lake group i in Table 1) the median of total phytoplankton biomass was Reference lakes were clustered on the axis 1 into four 0.44 mg 1-I (Fig. 3) and the chlorophyll a median 2.9 ktg distinct groups on the basis of phytoplankton assem- 1-1. Cyanobacteria contributed 6% to the total biomass

Table 2. Some characteristics of the studied impacted lakes. Lake No. = number of the lake in Fig. 1. Drainage basin numbers are given ac- cording to EKHOLM(1993). Description of lake groups: Lake group 1 = impacted oligo-humic large lakes; lake group 2 = impacted oligo-humic moderately large lakes; lake group 3 = impacted humic lakes. For further information, see the legend to Table 1.

Lake Lake Drainage TotP TotN Water colour pH Cyano Crypto Chryso group No. basin Pg I-1 tJg [-~ mg 1-1 Pt % % No. mg I-~ %

1 37 35.41 16 600 80 6.9 0.002 0.2 12 2 40 14.22 12 530 30 7.3 0.05 8 46 23 41 35.72 12 400 25 7.4 0.04 3 16 21 44 59.31 20 660 40 7.2 0.10 11 11 38 46 04.28 29 770 70 7.2 0.01 0.3 44 19 48 35.23 27 1200 60 7.7 0.48 13 8 2 49 35.22 17 450 15 7.3 0.39 13 26 20 51 34.03 24 440 20 8.0 0.04 5 14 9 52 35.21 35 670 40 7.8 1.00 28 23 5

2 33 35.77 10 410 25 7.6 0.04 5 7 46 34 35.71 12 330 20 7.5 0.06 7 18 21 35 35,23 28 540 35 7.7 0.44 29 11 13 36 35.81 50 640 90 7.6 0.22 6 9 9 42 14.18 11 600 45 7.3 0.03 5 19 40 45 35.18 30 690 40 7.2 0.17 3 3 2 50 35.73 11 370 20 7.3 0.09 10 8 29 53 35.83 13 1400 65 7.3 0.14 11 15 27 54 35.97 39 810 60 8.9 0.31 8 9 29

3 38 35.52 20 840 100 6.9 0.23 6 7 27 39 47.03 26 1000 80 7.2 1.16 35 8 I 43 35.25 52 1400 50 10.0 2.21 62 28 I 47 65.83 14 310 45 7.1 0.02 2 24 6 55 35.42 16 770 110 6.6 0.03 8 11 30

Limnologica (2004) 34,236-248 Type:specific and indicator taxa of phytoplankton 241 and cryptomonads (Cryptophycea) 14% as median val- gustissima and Rhizosolenia eriensis were type-specific. ues. The proportion of diatoms (Diatomophyceae) was In all studied oligo-humic large lakes, irrespective of 22% and that of chrysomonads (Chrysophyceae) 26%. their ecological status, the cyanobacteria Aphanothece Chloromonads (Raphidophyceae) were observed only minutissima, Snowella atomus and Woronichinia occasionally and the maximum percentage was 2% of naegeliana, and the medium-large (cell length 26 Fro) the total biomass (Table 1). Altogether 15 taxa were sta- cryptomonad Cryptomonas sp., diatoms Asterionella tistically selected as type-specific indicator taxa for high formosa and Tabellaria flocculosa and the green algae ecological status (90 th percentile) when using the cumu- Polytoma spp. and Botryococcus terribilis were fre- lative distribution function. Such algae as the cyanobac- quently observed (Fig. 4, Table 3). teria Merismopedia warmingiana and Anabaena lem- In oligo-humic, moderately large reference lakes mermannii and the small chrysomonads Chrysolykos (lake group 2 in Table 1) the total median biomass was planctonicus, Dinobryon borgei, D. crenulatum and D. 0.5 mg 1-1 and median chlorophyll a concentration was suecicum, and the dinoflagellate Peridinium umbonatum 3.2,u g 1-1. The total phytoplankton biomass included 7% belonged to these taxa (Fig. 4, Table 3). cyanobacteria, 19% cryptomonads, 7% diatoms and In impacted oligo-humic large lakes (lake group 1 in 25% chrysomonads. Altogether 14 taxa were statistical- Table 2) the median biomass was 1.25 mg 1-1 (Fig. 3) and ly selected as type-specific indicator taxa for high eco- the chlorophyll a concentration was 8.6 pg 1-1. logical status (90 th percentile) when using the cumula- Cyanobacteria contributed 8% (median value) to the tive distribution function (Fig. 5, Table 3). The cyano- total biomass, cryptomonads 16% and diatoms 31% bacteria Aphanothece clathrata, Chroococcus minutus (Table 2). The proportion of chrysomonads was 19% and Radiocystis geminata, the chrysomonads Dinobryon and that of chloromonads (Gonyostomum semen) 2% at borgei, D. crenulatum and Kephyrion boreale and the the highest, if present. Cyanobacterium Microcystis green algae Monoraphidium komarkovae and Oocystis viridis and the diatoms Aulacoseira granulata v. an- rhomboidea belonged to these taxa (Fig. 5, Table 3).

Table 2. (Continued)

Diatoms Raphi Total phytopl. Chlor. a Ecol. Classes Cyano Ecol. Classes Diatoms General water % biomass IJg I-~ quality mg I-~ % mgl -~ biomass % biomass % classification

0.60 81 0.80 6.7 high high bad poor good 0.10 18 0.58 4.4 good good high high good 0.65 52 1.25 8.6 good high bad moderate good O. 15 17 0.6 0.87 6.1 poor moderate good high good 0.50 30 1 1.67 8.8 high high bad good moderate 2.40 67 3.60 14.0 bad moderate bad poor moderate 0.94 31 2 3.07 6.9 bad moderate bad good moderate 0.55 57 0.96 12.0 good high bad poor good 1.80 31 3.53 27.0 bad poor bad good moderate

0.12 15 0.81 5.6 high high bad moderate excellent 0.19 22 0.86 5.4 good high bad poor good 0.44 30 1.51 11,0 bad poor bad poor good 1.93 53 11 3.63 36.0 bad high bad bad moderate 0.11 20 0.1 0.58 4.9 high high bad poor good 0.39 7 60 5.71 35.0 poor high bad high moderate 0.36 36 0.98 3.7 moderate good bad bad good 0.35 28 1.24 6.3 poor good bad poor good 1.81 44 0.1 4.07 26.0 bad high bad bad moderate

1.99 55 1 3.64 18.0 bad bad bad moderate good 1.75 52 3.34 12.0 bad bad bad moderate moderate 0.08 2 3.49 84.0 bad bad high high moderate 0.43 59 2 0.73 3.7 moderate moderate poor moderate moderate 0.12 34 3 0,36 4.7 poor bad good good good

Limnologica (2004) 34,236-248 242 L. Lepist6 et al.

SAAKSJAR • \,

Water PAlJ78 PO4P •ISO-HANH Ntot PtoL • VALKEA-K A HAUKKAJ )/ KALLIOJ ~ANATTI KUOUMO VUOHUAR • UNARII • KUKKIA PIELINEA •

PIHLAJA Axis 1

ISO LOYT • • VEHI ISO-HIET• • NASIJ • ISO-ARAJ

SIIKAJARVI • Fig. 2. Dedrended correspondence analysis (DCA) of phytoplankton PuuJARVl • sampling sites. Eigen values for axis 1 = 0.55, and for axis 2 = 0.3. IKATTI LAJ 2 Lake group 1 = oligo-humic large lakes; lake group 2 = oligo-humic \ • moderately large lakes; lake group 3 = humic lakes; lake group 4 = dystrophic lakes; lake group 5 = dystrophic acidic lakes.

12 The median biomass in impacted moderately large reference lakes (lake group 2 in Table 2) was 1.24 mg 1-1 and medi- U impacted an chlorophyll a 6.3 ,ug 1-]. Cyanobacteria contributed 10 7% (median value), cryptomonads 9% and diatoms 28% to the total biomass. The proportion of chrysomonads was 27%. The maximum percentage of chloromonads was 60%. The cyanobacterium Aphanocapsa holsatica, and the diatoms Acanthoceras zachariasii, Aulacoseira ambigua, A. granulata, A. italica, A. italica var. tenuissi- o_E ma and A. tenella represented type-specific taxa. Fur- .13 thermore, the green alga Dictyosphaerium subsolitarium was also type-specific in impacted lakes. Indifferent iiiiiii~!i taxa, occurring in both reference and impacted lakes, were the medium-large Cryptomonas spp., Ceratium

ii:~!!!!!!!. hirundinella, Mallomonas akrokomos and Botryococcus terribilis (Fig. 5, Table 3).

?i;'ii]i[ii~ [] Fig. 3. The total phytoplankton biomass in reference and impacted lakes as ,ii i i i i N= 14 9 10 9 36 5 2 box-plot figures. The minimum, maximum, median and deviation values are 1 2 3 4 5 given. N = the number of observations; reference = reference lakes; impacted = Lake groups impacted lakes.

Limnologica (2004) 34,236-248 Type-specific and indicator taxa of phytoplankton 243

• Humic lakes In the impacted humic lakes (lake group 3 in Table 2) In humic reference lakes (lake group 3 in Table 1) the the median biomass was 3.34 mg 1-1 and chlorophyll a median biomass was 0.95 mg 1-1 and the median of concentration was 12 ktg 1-1. The median proportion of chlorophyll a was 8.2 Mg 1-1. Cyanobacteria contributed cyanobacteria was 8%, of cryptomonads 11% and of di- 1% to the total biomass and cryptomonads 7%. The me- atoms 52%. Chrysomonads contributed 6% and chloro- dian proportion of diatoms was 25% and chloromonads monads a maximum of 2% to the total biomass. The 31% of the total biomass. Chrysomonads contributed cyanobacteria Aphanothece minutissima and Anabaena 11% (Table 1). Altogether 9 taxa were statistically se- spp. (twisted) and the diatom Rhizosolenia eriensis were lected as type-specific indicator taxa for high ecological type-specific. Indifferent were the frequently observed status (90 th percentile) when using the cumulative distri- chrysomonads Dinobryon bavaricum and Mallomonas bution function (Fig. 6, Table 3). No cyanobacteria were caudata and the diatoms Asterionella formosa and type-specific but the chrysomonads Bicosoeca spp. and Tabellaria flocculosa. The chloromonad Gonyostomum Dinobryon divergens, the diatom Aulacoseira ambigua, semen was moderately frequently observed (Fig. 6, the heterocontae Tetraedriella jovetii and the green alga Table 3). Pseudosphaerocystis lacustris belonged to these taxa Two dystrophic, extreme lakes, Lake Lika-Pytree (Fig. 6, Table 3). (lake No. 9), a small, shallow and "naturally eutrophic"

Table 3. Alphabetic list of type-specific species presented in Figs. 4-6 by RUBIN codes (ZE]qERBERG1986).

RUBIN code Scientific name RUBIN code Scientific name

Acan zac Acanthoceraszachariasfi (BRUN.) SiMONSEN Gloe liy G/oeobotrys limneticus(G.M. SMITH)PASCHER Anab lem Anabaena lemmermannfiR RICHTER Gony sem Gonyostomumsemen (EHR.) DIESING Anabanaz Anabaena spp. (twisted) Keph bor Kephyrion boreale SKUJA Anky lan Ankyra lanceolata(KORSH.) FOTT Keph cup Kephyrion cupuliformeCONRAD Apha hol Aphanocapsa holsatica(LEMM.) CRONBERG & KOMAREK Keph ova Kephyrion ovale (LACK.) HUBER-PESTALOZZl Apha cla Aphanothece clathrataW, et G.S. WEST Keph sku Kephyrion skujai ETTL Apha min Aphanothece minutissimaKOM.-LEG, & CRONBERG Mall akr Mallomonas akrokomosRUTTNER Aphanizz Aphanizomenonspp. Mall cau Mallomonas caudata IVANOVem. KRIEGER Aula arab Aulacoseira ambigua (GRUNOW)SIMONSEN Meri war Merismopedia warmingiana LAGERHEIM Aula gra Aulacoseira granu/ata (EHR.) StMONSEN Micr plu Micractinium pusillum FRESENIUS Au gr; an Aulacoseira granu/atav. angustissima(O.M.) SIMONSEN Micr vir Microcystis viridis (A.BR.) LEMMERMANN Aula ita Aulacoseira italica (EHRENBERG)SIMONSEN Monomasz Monomasfixsp. Au it; te Aulacoseira italica v. tenuissima(GRUNOW) SIMONSEN Mono dyb Monoraphidium dybowskfi(WOE.) HIND.& KOM.-LEG. Aula ten Aulacoseira tenella (NYGAARD)SIMONSEN Mono kom Monoraphidium komarkovae NYGAARD Aste for Astefionella formosa HASSALL Nitz aci Nitzschia acicularisW. SMITH Bicosoez Bicosoecasp. Oocy rho Oocystisrhomboidea FOTT Bico mit Bicosoeca mitra FOTT Peri umb Peridinium umbonatumSTEIN Botr ter Botryococcus terribilis KOMAREK& MARVAN Polytomz Polytoma spp. Cera hir Ceratium hirundinella (O.EM.) SCHRANK Pseu lac Pseudosphaerocystislacustris (LEMM.) NOVAKOVA Cera foi Ceratium furcoides(LEVANDER) LANGHANS Pseu ent Pseudokephyrionentzii (CONRAD)SCHMID Chro mts Chroococcusminutus (KOTZlNG)N~,GELI Quad pfi Quadrigu/apfitzeri (SCHRODER)G.M. SMITH Chry pla Chrysolykosplanctonicus MACK Radi gem Radiocystisgeminata SKUJA Clos gra CIosteriumgracile BR~BISSON Rhab dli Rhabdodermalineare SCHMIDLE& LAUTERBORN Cryptomz Cryptomonasspp. (cell length <13 pro; 26 pm) Rhiz eri Rhizosoleniaeriensis H.L. SU ITH Dict sub Dictyosphaeriumsubsolitarium VAN GOOR Rhodomoz Rhodomonasspp./ Plagiose/mis spp. Didymocz Didymocystisspp. Scen arm 5cenedesmusarmatus CHODAT Dino bav Dinobryon bavaricum IMHOF Scourfiz Scouffieldia sp. Dino bor Dinobryon borgei LEMMERMANN Snow ato Snowella atomus KOMAREK& HINDAK Dino cre Dinobryon crenulatumW. & &&WEST Stepdisz 5tephanodiscusspp. Dino div Dinobryon divergens IM HO F Synura z Synuraspp. Dino sue Dinobryon suecicum LEMMERMANN Tabe rio Tabellaria flocculosa (ROTH)KOTZlNG Elak gel ElakatothrixgelatinosaWILLE Tetr jov Tetraedriel/ajovetii (BOURRELLY)BOURRELLY Frag cro Fragilaria crotonensisKITTON Uroglenz Uroglena spp. Frag uln Fragilaria ulna (NITzSCH)LANGE-BERTALOT Woro nae Woronichinia naegeliana(UNGER) ELENKIN

Limnologica (2004) 34,236-248 244 L. Lepist6 et al.

Oocy rho 9/3 ' Dino cre 1311 ~;~ Dino bor 8/3 Dino bor 12/2 q!~ • ~ D[no cre 8/3 Dino sue 9/1 " Mono kom 3/1}~ Men• war 9/ 1~ Kephy bor 3/0 '~!~ Anab lem 8/0 Apha hol 0/7 Keph bor 7/1 Apha cla 3/0 '~i~ can zac 0/7 Gloe liy 2t0 Keph ova 7/1 '~ la arab 0/7 Radi gem 2/0 ~'i~ Peri urnb 6/1 i',~" t;te 0/7 Bicosoez 0/3 Tabe flo 612 !:~, Keph sku 5/0 ub 0/6 epdisz 0t3 Chro rots 3/1 q "L ~' Aula ita 0/5 Quad pfi 5/0 ~'i~ gr;an 0/2 Pseu ent 3/1 jr Aula ten 0/5 Chry pla 5/1 ~:I':~ gra 0/2 Tetr rain 3/1 !i, V Frag uln 0/5 Keph cup 4f0 ~ plu 0/2 L Rhab dli 2/0 '~ Aula gra 0/4 Cera foi 4/0 i 0/2 Pseu ent 8/2 !'i O/2 Mono dyb 10/6 I~ Oocy rho 4/1 '~',~ 3cen arm 0/2 Mall akr 10/6 !~ Cryptomz (26 pm) 13/9 ~ Cryptomz (26 IJrn) 9/8ii Snow ato 15/8 Botr ter 8f7 Mono dyb 14/9 Cera hir 8t6 I~ Rhodomoz 1419 Fig. 5. Type-specific and indicator species (taxa) for oligo-humic Uroglenz 14/8 moderately large reference (left) and impacted lakes (right) are pre- Aste for 13/9 sented as RUBIN codes. Scientific names are given in Table 3. Number Polytornz 13t9 of observed taxa in reference lakes/impacted lakes is indicated. Indif- Tabe flo 13/9 ferent species (taxa) are situated below. The total number of refer- Woro nae 13/9 ence lakes was ten and of impacted lakes nine. Apha min 1318 ~: Botr ter 13/5

Fig. 4. Type-specific and indicator species (taxa) for oligo-humic Apha min 0t5 large reference (left) and impacted lakes (right) are presented as '{ Anabanaz 0/4 RUBIN codes. Scientific names are given in Table 3. In connection Aula amb 2/0 ~, Rhiz eri 0/3 with RUBIN code is indicated the number of observations of the Bicosoez 2/0 Woro nae 1/5 taxon in reference lakes/impacted lakes• Indifferent species (taxa) are Dino div 2/0 '¢ JJ~,nky lan 1/4 situated below. The total number of reference lakes was fifteen and Tetr jov 2/0 ~ /J~,phanizz 1/4 that of impacted lakes nine. Monomasz 3/1 ~ /Cryptomz (26 prn) 1/4 Cryptomz (<13 tJm) 2/1 Didymocz 1/4 Bico mit 2/1 E[ak gel 1t4 Pseu lac 2/1 ,~ Frag cro 1/4 lake, and Lake Kallioj~irvi (lake No. 16) with an occa- Scourfiz 2/1 ',~'Snow ato 1/4 sional biomass maximum, formed a separate group (lake group 4 in Table l). Chloromonads (Gonyostomum Mall cau 3/4 and diatoms such as con- semen) Tabellaria flocculosa Synura z 3/4 tributed 31-68% and 2-70%, respectively, to the total Aste for 3/4 biomass (Tables 1 and 4). In two lakes (lake group 5 in Tabe flo 3/4 Table 1) the acidic, humic Lake Valkea-Kotinen (lake Dino bav 3/3 No. 6) and the acidic, dystrophic Lake Iso-Hanhij~vi Aula ten 3/2 (lake No. 13) the biomasses were 0.30 and 0.88 mg lq Gony sem 3/2 and the chlorophyll a concentrations were 12 and 4.9 iug Dino bor 3/2 1q, respectively. The main part of the biomass was com- Mall pun 3/2 posed of dinoflagellates. Typical taxa in these lakes are Spinifez 3/2 Gonyostomum semen, Gymnodinium spp., Peridinium Fig. 6. Type-specific and indicator species (taxa) for humic reference spp. and spp., umbonatum, Monochrysis Spiniferomonas (left) and impacted lakes (right) are presented as RUBIN codes. Scien- as well as Pseudopedinella spp. (Table 4). No impacted tific names are given in Table 3. Number of observed taxa in reference lakes in this data were comparable to these four lakes, lakes/impacted lakes is indicated. Indifferent species (taxa) are situat- i.e. lakes Lika-Py6ree, Kallioj~vi, Valkea-Kotinen and ed below. The total number of reference lakes was three and of im- Iso-Hanhij~-vi. pacted lakes five.

Limnologica (2004) 34,236-248 Type-specific and indicator taxa of phytoplankton 245

Table 4. Typical species (taxa) for dystrophic and dystrophic acidic reference lakes.

Dystrophic reference lakes Dystrophic acidic reference lakes (Lakes Lika-Py6ree and Kalliojfirvi) (Lakes Valkea-Kotinen and Iso-Hanhij~rvi)

Bitrichia chodatii (REVERDIN)HOLLANDE Gonyostomumsemen (EHR.) DIESlNG Dinobryon borgei LEMMERMANN Gymnodiniumsp. Gymnodiniumsp. Peridinium umbonatumSTEIN Peridinium umb, v. goslaviense(WOL.) POPOV.& PFIEST. Dinobryon bavaricumIMHOF Gonyostomumsemen (EHR.) DIESlNG Monochrysisspp.

Preliminary determination of ecological status Discussion

The ecological status of 23 impacted oligo-humic and The total phosphorus concentration, the median biomass humic lakes was determined preliminarily using the and the chlorophyll a concentration indicated oligotro- EQR-ratios of 0.8 for high, 0.6 for good and 0.4 for phy in large oligo-humic reference lakes, according to moderate as boundaries between classes. the limits specified by HEINONEN (1980) for Finnish lakes and by OECD (1982). This agrees with the nation- • Cyanobacteria EQR al water quality classification in Finland, in which only The EQR-ratio based on the median cyanobacteria 4% of the lake area was significantly impacted by local biomass classified two of the oligo-humic large lakes to water pollution (VUORISTO 1998). The total phosphorus high, three to good and four to poor or bad ecological concentration reflected mesotrophy and the biomass was status. The percentage of cyanobacteria, however, re- almost fourfold higher in the impacted lakes. Cyanobac- flected high or good status for five of these lakes. In teria increased slightly in impacted lakes whereas oligo-humic moderately large lakes the cyanobacteria chrysomonads slightly decreased. In moderately large biomass EQR indicated in two lakes high, in one good reference lakes the median biomass was higher than in and in six moderate - bad ecological status but the EQR- large reference lakes, being close to oligo-mesotrophic ratio on the basis of cyanobacteria percentage indicated concentrations, which is in accordance with the observa- high or good ecological status with the exception of one tions of FEZ et al. (1992). Human impact increased the lake with poor status. Four humic lakes had poor or bad ecological status median biomass twofold in these lakes. The proportion and in one lake the cyanobacterial biomass EQR indicat- of cryptomonads was reduced clearly but the proportion ed moderate ecological status. The EQR-ratio based on of diatoms was increased threefold in impacted lakes median cyanobacteria percentage indicated bad ecologi- compared to reference lakes. cal status in four lakes with the exception of the man- The filamentous cyanobacterium Anabaena lemmer- made lake with moderate status (Table 2). mannii, considered as typical for oligotrophic waters (LEPIST0 1999), was clearly type-specific for large oligo- • Diatom EQR humic reference lakes but was not observed in impacted The diatom biomass EQR-ratio classified seven of nine large lakes in this study. It has not been included in An- oligo-humic large lakes as bad and two as having high or abaena spp. identified in the impacted lakes. Several good ecological status. However, when using the EQR- small-celled species, such as Merismopedia warmin- ratio of the percentage of diatoms, five lakes had high or giana, Dinobryon borgei, D. suecicum, and Kephyrion good ecological status and four lakes had moderate or spp. were also type-specific. Radiocystis geminata, Ke- poor ecological status. In all moderately large oligo- phyrion boreale and Oocystis rhomboidea were type- humic lakes the diatom biomass EQR indicated bad eco- specific for moderately large lakes. The species list logical status but the EQR-ratio on the basis of diatom agrees with the observations of assemblages typical for percentage indicated high or moderate ecological status oligotrophic and oligo-mesotrophic waters (WmLgN in two lakes and poor or bad status in seven lakes (Table 1992; LEPIST0 1999; REYNOLDS et al. 2002). According 2). to the Water Framework Directive (European Union Two humic lakes had high or good and three lakes had 2000), phytoplankton assemblages in waters with high a poor or bad ecological status according to the diatom ecological status should be composed mainly of taxa biomass EQR-ratio. By contrast, the percentage EQR re- type-specific for reference conditions and with almost no flected high or good for two lakes and moderate status taxa typical for impacted waters. In the studied oligo- for three lakes. humic lakes type-specific indicator taxa for high ecologi-

Limnologica (2004) 34,236-248 246 L. Lepist6 et al.

cal status, and type-specific taxa for impacted lakes with particles and bacteria (SALONEN~1; JOKINEN 1988; HOL~N mainly good or moderate ecological status were deter- & BORAAS 1996). For example, Gonyostomum semen is mined and several taxa were also found to be indifferent. able to respond to low light conditions and to occasional With impairment of the ecological status, the often nutrient depletion by its migrative behavior and by large-sized, type-specific taxa for impacted waters tend mixotrophy (SALONEN et al. 1984; JANSSONet al. 1996). to become dominant. Such an increase of large-sized In the study lakes this species was observed in dystroph- taxa was reported by WmI.~N (1992) in the Swedish ic reference lakes with low pH, which agrees with the lakes during the process of eutrophication. Microcystis observations of CRONBERGet al. (1988). viridis, Aulacoseira granulata v. angustissima and Rhi- The ecological classification of the study lakes was zosolenia eriensis were type-specific in impacted oligo- generally in agreement with earlier information presented humic large lakes whereas in moderately large lakes e.g. by VUORISTO(1998), especially in the case of cyanobacte- Acanthoceras zachariasii, Aulacoseira ambigua and A. rial biomass but less clearly as cyanobacterial biomass italica v. tenuissima were the type-specific taxa. percentage. Neither the biomass nor the percentage of di- The mesotrophy-indicating median biomass, accord- atoms agreed with the earlier water quality classification. ing to HEINONEN (1980) in humic reference lakes was in This observation should be more carefully considered, as accordance with earlier observations from humic lakes one of the methods to assess the approximate original with high biomass values produced by cryptomonads, ecological status of naturally eutrophic lakes are the pale- diatoms, and by Gonyostomum semen (ARVOLA 1984; olimnological studies based on diatom assemblages. SALONEN et al. 1992; SAI.O~N et al. 2001). In impacted However, the preliminary combination of indicative pa- humic lakes the median biomass was three times higher, rameters by averaging (Ecostat 2003), to estimate the and the proportion of diatoms was twice as high as in ecological status of the studied impacted lakes was in reference conditions. This was the case especially in a general in accordance with the water quality classifica- man-made lake in which regulation of the water level is tion of Finnish waters presented by VuoRIsro (1998). reflected in the abundance of diatoms in the overall phy- Finally, we want to underline that the attempt to group toplankton biomass (LEPIST0 & PIETILXlNEN 1996), the lakes, even those of the same type, in order to find which is however rather low compared to the other im- out type-specific species is hazardous and the list of pacted humic lakes. Interestingly, the diatom Aulaco- type-specific taxa needs further evaluation. As ROUND seira ambigua, which was reported by BRETTUM(1989) (1981) has demonstrated, no two lakes are alike, and to indicate mesotrophic conditions, was type-specific therefore no floras are alike, although there are certain for impacted oligo-humic lakes, but also for humic ref- broad categories of lakes with similar basic conditions. erence lakes. The fragile diatom Rhizosolenia eriensis, reported to decrease with increasing eutrophication (DAVIS 1964), was detected in oligo-humic and in humic Concluding remarks impacted lakes as type-specific. WII~LEN (2003) report- The type-specific taxa for reference conditions as indica- ed this species as a characteristic of humic reference tors for high ecological status in oligo-humic waters forest lakes in Sweden. In the studied humic lakes indi- were taxa reported to indicate oligotrophic conditions. cator species for high ecological status, and for impact- These taxa should be present at least by 50% in waters ed lakes with mainly good or moderate ecological status having a high ecological status. Some taxa were typical were determined and several taxa were classified as in- for impacted waters. Furthermore, there are numerous in- different. different taxa. Interestingly, some taxa type-specific for Lakes Lika-Py6ree (No. 9) - a small, shallow and impacted oligo-humic lakes proved to be the type-specif- "naturally eutrophic" lake - and Kallioj~rvi (No. 16) ic taxa for humic reference lakes. formed a separate group. Gymnodinium spp., Peridinium When the lakes are correctly grouped into lake types goslaviense, Bitrichia chodatii, Dinobryon borgei, and and into reference and impacted lakes, the taxa list the chloromonad Gonyostomum semen were type-spe- agrees with the observations of phytoplankton assem- cific but diatoms were also abundant in these lakes. This blages in lakes of e.g. various trophic status and water observation agrees with the main species assemblages colours. This result is also in accordance with our long- from Swedish humic forest lakes (WlLL~N 2003). In dys- time observations from phytoplankton assemblages in trophic acidic lakes the biomass values are clearly high- boreal lakes. er compared to those in oligo-humic acidic lakes report- ed by KIPPO-EDLUND& HEITTO (1990), obviously due to the abundant humic substances (ARVOLA1984; SALONEN Acknowledgements et al. 2001) and to the heterotrophic or mixotrophic be- haviour of the main part of the type-specific flagellate d The authors thank Reija Jokipii and Maija Niemel~i for the algae. These organisms are able to ingest both organic analysis of phytoplankton samples, Ansa Pilke for valuable

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