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The ecology of the invasive cyanobacterium Cylindrospermopsisraciborskii (Nostocales, Cyanophyta) in two hypereutrophic lakesdominated by Planktothrix agardhii (Oscillatoriales, Cyanophyta)Mikołaj Kokocińskiab; Karolina Stefaniakb; Joanna Mankiewicz-Boczekc; Katarzyna Izydorczykc; JanneSoininend

a Collegium Polonicum, Adam Mickiewicz University, 69-100 Słubice, Poland b Faculty of Biology,Adam Mickiewicz University, Poland c International Institute of the Polish Academy of Sciences -European Regional Centre for Ecohydrology u/a UNESCO, Tylna 3, 90-364 Łódź, Poland d Departmentof Environmental Sciences, University of Helsinki, Finland

First published on: 21 September 2010

To cite this Article Kokociński, Mikołaj , Stefaniak, Karolina , Mankiewicz-Boczek, Joanna , Izydorczyk, Katarzyna andSoininen, Janne(2010) 'The ecology of the invasive cyanobacterium Cylindrospermopsis raciborskii (Nostocales,Cyanophyta) in two hypereutrophic lakes dominated by Planktothrix agardhii (Oscillatoriales, Cyanophyta)', EuropeanJournal of Phycology, 45: 4, 365 — 374, First published on: 21 September 2010 (iFirst)To link to this Article: DOI: 10.1080/09670262.2010.492916URL: http://dx.doi.org/10.1080/09670262.2010.492916

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Eur. J. Phycol. (2010) 45(4): 365–374

The ecology of the invasive cyanobacterium Cylindrospermopsis

raciborskii (Nostocales, Cyanophyta) in two hypereutrophic

lakes dominated by Planktothrix agardhii (Oscillatoriales,

Cyanophyta)

MIKOLAJ KOKOCINSKI1,2, KAROLINA STEFANIAK2, JOANNA MANKIEWICZ-BOCZEK3,

KATARZYNA IZYDORCZYK3 AND JANNE SOININEN4

1Collegium Polonicum, Adam Mickiewicz University, ul. Kosciuszki 1, 69-100 Slubice, Poland2Faculty of Biology, Adam Mickiewicz University, Poland3International Institute of the Polish Academy of Sciences – European Regional Centre for Ecohydrology u/a UNESCO, Tylna 3,

90-364 L=odz, Poland4Department of Environmental Sciences, University of Helsinki, Finland

(Received 23 October 2009; accepted 10 May 2010)

Biological invasions have attracted particular attention since they often result in serious consequences for natural ecosystems.

One planktonic invasive species is Cylindrospermopsis raciborskii, a cyanobacterium originally reported to occur exclusively

in the tropics. Over the last few decades its range has extended to temperate regions and it occupies shallow highly eutrophic

lakes previously dominated by other cyanobacteria. The purpose of this study was to examine the ecology of C. raciborskii

during Planktothrix agardhii blooms in two shallow lakes in western Poland and to determine whether these species have

different environmental preferences. Multiple linear regression showed that the biomass of P. agardhii was significantly

negatively related to Secchi depth in Lake Bninskie. In Lake Bytynskie, P. agardhii was significantly positively related to

concentrations of PO3�4 , chlorophyll a and total phosphorus and negatively related to Secchi depth, NO�3 , and total nitrogen.

Cylindrospermopsis raciborskii was significantly positively related only to concentrations of NHþ4 . There was a negative

correlation between the biomass of P. agardhii and C. raciborskii perhaps showing different responses to environmental

variables. Moreover, the biomass of P. agardhii was negatively correlated with Shannon–Wiener diversity of the phyto-

plankton assemblages. Our results support the concept that these cyanobacterial species have different environmental pref-

erences and their niches differ from each other. These results suggest that light is an important driver of phytoplankton

community structure resulting in shifts from a community dominated by P. agardhii in very turbid waters to more diverse

communities perhaps including the invasive C. raciborskii in clearer waters.

Key words: biological invasions, Cylindrospermopsis raciborskii, environmental factors, phytoplankton, Planktothrix agardhii,

shallow lakes

Introduction

Biological invasions are considered a major threatto global biodiversity and are an important part ofongoing global climate change. The number ofinvasions has grown considerably in recent dec-ades, many of them driven by human activitiesthat diminish natural barriers to dispersal (Wellset al., 1986; Dukes & Mooney, 1999). At presentonly a few habitats remain free of species intro-duced by humans (Fridriksson & Magnusson,1992). Ecological consequences of biotic invasionsvary enormously, but they often result in the

altered identity and functioning of natural commu-nities (Mack et al., 2000). Invaders may severelyaffect the ecosystems by modifying the speciesdominance structure, nutrient dynamics andlevels of primary productivity (Bertness, 1984;Vitousek, 1990).Successful invasions accompany the major com-

ponents of global change that include increasingtemperatures (Walther, 2003), nitrogen deposition,and CO2 concentration, plus changing patterns ofland use or disturbance regimes (Dukes &Mooney, 1999). Aquatic ecosystems are especiallysensitive to these changes, which often includemore frequent cyanobacterial blooms. Rising tem-peratures favour cyanobacteria both directly, as

Correspondence to: Mikolaj Kokocinski. E-mail:

kok@amu.edu.pl

ISSN 0967-0262 print/ISSN 1469-4433 online/10/04000365–374 � 2010 British Phycological Society

DOI: 10.1080/09670262.2010.492916

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they grow faster at higher temperatures during per-iods of water stratification, and indirectly bychanging patterns of precipitation and drought(Paerl & Huisman, 2008). These changes mayalso allow for the establishment of invasive cyano-bacterial species.Among the many examples of biological inva-

sions is the expansion of the cyanobacteriumCylindrospermopsis raciborskii (Woloszynska)Seenayya & Subba Raju in temperate aquatic eco-systems. This species, common in the tropics, hasbeen observed in temperate regions over the lasttwo decades (Padisak, 1997; Wiedner et al., 2002;Saker et al., 2003; Manti et al., 2005). Recently, itwas found in shallow, eutrophic, polymictic lakesof the Wielkopolska region in western Poland,often co-occurring with the native speciesPlanktothrix agardhii (Gomont) Anagnostidis &Komarek (Stefaniak & Kokocinski, 2005). Thesespecies are planktonic, filamentous cyanobacteriabelonging to the Nostocales and Oscillatoriales,respectively. Both species are of great concerndue to their ability to produce toxins harmful tohumans and animals. Planktothrix agardhii isknown for producing a variety of microcystins(Carmichael, 1994; Chorus, 2001), while C. raci-borskii is able to synthesize the neurotoxin saxi-toxin (Lagos et al., 1999; Castro et al., 2004) andthe alkaloid hepatotoxin cylindrospermopsin(Ohtani et al., 1992; Li et al., 2001).Although C. raciborskii and P. agardhii are able

to grow under varied conditions, their environmen-tal requirements probably differ. Temperature hasbeen considered the major limiting factor forgrowth of C. raciborskii (Padisak, 1997; Wiedneret al., 2007), with its optimal growth rate in labo-ratory experiments being at 25–35�C (Saker &Griffiths, 2000; Briand et al., 2004; Castro et al.,2004; Chonudomkul et al., 2004). Furthermore, itsakinete germination is temperature dependent, andgermination occurs primarily from 22–23.5�C(Padisak, 1997). In contrast, P. agardhii can growwell at much lower temperatures, 6–16�C (Berger,1989; Dokulil & Teubner, 2000) and long-lastingpopulations have been observed in highly eutro-phic reservoirs even during winter (Berger, 1975;Post et al., 1985; Nixdorf, 1994; Poulickovaet al., 2004). Nonetheless, it is well known thatP. agardhii populations develop optimally in latesummer or autumn, because it prefers warm watersabove 20�C (Van Liere & Mur, 1980; Ramberg,1988).Population densities of phytoplankton species

are also affected by light intensity. Based on earlierfindings, it was suggested that C. raciborskii canbenefit from low light intensities (Dokulil &Mayer, 1996; Padisak & Reynolds, 1998; Bouvyet al., 1999; Briand et al., 2002b; Mischke &

Nixdorf, 2003). However, recent experimentalstudies on tropical and temperate C. raciborskiiisolates showed no significant differences ingrowth rates at different light intensities (Briandet al., 2004). Planktothrix agardhii is also associ-ated with turbid waters, and is a common species inshallow, polymictic lakes with high disturbance fre-quency (Rucker et al., 1997; Scheffer et al., 1997;Nixdorf et al., 2003). Light and temperature andtheir interactions are currently gaining attentionsince global warming has increased water temper-atures in lakes during spring in addition to alteringphysical conditions (George et al., 2000; Gerten &Adrian, 2000). Moreover, relationships betweentemperature and photoperiod linked to climatewarming may influence phytoplankton composi-tion (Nicklisch et al., 2008).Nutrient concentrations also have a role in

structuring phytoplankton communities.Cylindrospermopsis raciborskii is characterized byits association with high TN/TP ratios (Briandet al., 2002b), while P. agardhii appears to befavoured by low TN/TP ratios (Rucker et al.,1997). Moreover, both species are able to developvery abundant populations or even form intenseblooms (Berger, 1975, 1989; De Souza et al.,1998; Fonseca & De M. Bicudo, 2008).Occurrence of C. raciborskii with mass develop-ment of P. agardhii is known in Polish lakes(Stefaniak & Kokocinski, 2005; Pelechata et al.,2006; Kokocinski et al., 2009) but documentedexamples of abundant coexistence of these speciesare sparse (Mischke & Nixdorf, 2003; Crossetti &De M. Bicudo, 2008).Although the autecology of these species is now

better known, the relationships between their envi-ronment and their occurrence in temperate lakes isless understood. Therefore, the objectives of thisstudy are: (i) to examine which environmental fac-tors drive the temporal patterns in phytoplanktoncommunities in the two lakes studied; (ii) to exam-ine which environmental factors control C. raci-borskii and P. agardhii concentrations andwhether the species respond differently to environ-mental factors; and (iii) determine whether thesetwo species coexist or show clear negative correla-tions in their abundances. We predict that growthof C. raciborskii will be favoured by high temper-atures and high light intensities, while P. agardhii isassociated with reduced light intensities and lowertemperatures (Fig. 1).

Materials and methods

Sampling sites

The study was conducted in two lakes, Bninskie (here-after ‘Lake BN’) and Bytynskie (hereafter ‘Lake BY’),

M. Kokocinski et al. 366

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located near the city of Poznan in the Wielkopolskaregion of western Poland. Both lakes are shallow (max-imum depth 58.5m), polymictic and highly eutrophic,surrounded by agricultural catchments, with public rec-reational usage. Their average depths are 4.2 and 3.5mrespectively, with other features given in Table 1.

Sampling

Sampling was carried out twice a month from July toOctober each year from 2004 to 2007. Altogether 32 sam-ples were collected from each lake during the study. As nothermal or oxygenation stratification was observed, andfollowing previous studies in shallow lakes (Berger, 1975;Romo & Miracle, 1993, 1994; Briand et al., 2002a; Ottet al., 2003) phytoplankton samples were collected from0.5m below the surface of the water. Samples for phyto-plankton and chemical analysis were collected using a 5 lLimnos water sampler at the deepest point of thereservoir. The phytoplankton samples were fixed withacidified Lugol’s solution (Wetzel & Likens, 2000)immediately after sampling. Then, formaldehyde wasadded as a preservative and samples were stored undercool and dark conditions until counted. Before counting,samples were sedimented in a 1 l glass cylinder for 48 h,after which the overlying water was gently decanted offand the lower layer (volume 40ml) was used for phyto-plankton analyses.

Phytoplankton analysis

Phytoplankton identification and counts were conductedusing a Zeiss light microscope (magnification 400�).

The phytoplankton counts were carried out in 160fields of the Fuchs-Rosenthal chamber, which ensuredthat at least 400 specimens were counted to reduce theerror to less than 10% (P¼ 0.05; Javornicky, 1958).Single cells, coenobia or filaments were considered asone specimen in this study. We assumed 100mm to bethe standard length for filaments and 100 cells the sizeof large spherical colonies. The biovolume of each specieswas determined via volumetric analysis of cells using geo-metric approximation and expressed as wet weight fol-lowing Hindak (1978) and Wetzel & Likens (2000). Foreach species geometrical dimensions of at least 30 indi-viduals were measured to obtain amean value. The diver-sity was calculated using the Shannon–Wiener diversityindex (Shannon, 1948) based on phytoplankton biomass.

Chemical and physical analysis

Water samples for chemical analyses were collected atthe same time as the phytoplankton samples, and wereanalysed for ammonium nitrogen (NHþ4 ), nitrate nitro-gen (NO�3 ), nitrite nitrogen (NO�2 ), total nitrogen (TN),orthophosphate phosphorus (PO3�

4 ) and total phospho-rus (TP) by using a HACH Spectrophotometer. Forchlorophyll a (chl a) analysis, 200ml of water was fil-tered through a GF/C Whatman filter. The concentra-tion was determined spectrophotometrically followingthe Lorenzen method after 90% acetone extractionand corrected for phaeopigments (Wetzel & Likens,2000). During field sampling, water temperature, pHand conductivity were determined using a multipara-meter Elmetron CPC-401 probe. Water transparencywas measured each time using a Secchi disc.

Statistical analyses

Prior to analyses, rare phytoplankton taxa, i.e. thosethat occurred in only one sample, were excluded fromthe ordinations. Environmental variables (except pH)were log-transformed to better approximate multivariatenormality. We first used canonical correspondence anal-ysis (CCA) to examine the temporal patterns of theentire phytoplankton community along major environ-mental gradients. CCA is a direct gradient analysis thatuses both species and environmental data by combiningordination and regression techniques (Ter Braak, 1986;Legendre & Legendre, 1998). We used forward selectionof environmental variables. At each step, only variablessignificantly (P50.05; Monte Carlo randomization testwith 499 permutations) related to assemblage structurewere included in the model. CCA was run usingCANOCO version 4.0 (Ter Braak & Smilauer, 1998).

We then analysed more closely which of the environ-mental variables were controlling the P. agardhii andC. raciborskii populations by using stepwise multipleregression. We used the probability level of 0.05 as thelimit for entry into the model. Before analysis, weexcluded variables that showed strongest (r40.80)co-linearity with other variables.

Spearman correlation analysis was carried out usingStatistica 7.1 to examine the correlation between bio-mass of P. agardhii and C. raciborskii. We then related

dominates

P. agardhiidominates

Temperature

Lig

ht

Coexistence

C. raciborskiidominates

P. agardhiidominates

Fig. 1. Conceptual model of the relationship betweenPlanktothrix agardhii and Cylindrospermopsis raciborskiiwith regard to temperature and light.

Table 1. Physical characteristics of Lake Bninskie (BN)

and Lake Bytynskie (BY) in western Poland.

Lake BN Lake BY

Latitude 52�12.7 52�30.5

Longitude 17�06.8 16�30.1

Area (ha) 225.9 308.8

Max. depth (m) 8.5 7.0

Average depth (m) 4.2 3.5

Max. width (m) 655 1490

Max. length (m) 4545 4160

Length of shore line (m) 11830 17475

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the biomass of P. agardhii to phytoplankton speciesrichness using linear regression analysis.

Results

Throughout the study in both lakes the phyto-plankton communities were dominated by cyano-bacteria which contributed over 80% of the totalphytoplankton biomass in most of the samples

(Figs 2–5). Planktothrix agardhii was the dominantspecies in both lakes with Limnothrix redekei (VanGoor) Meffert being subdominant. Beside thesetwo species, other common cyanobacteria in thesamples were Pseudanabaena limnetica(Lemmermann) Komarek (Oscillatoriales) andAphanizomenon flos-aquae Brebisson ex Bornet &Flahault, Aphanizomenon gracile Lemmermannand C. raciborskii (Nostocales).

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Fig. 3. Biomass of Planktothrix agardhii and Cylindrospermopsis raciborskii in Lake Bninskie from July to October in theyears 2004–2007.

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Bacillariophyceae Cyanophyta Chlorophyta ChrysophyceaeCryptophyta Dinophyta Euglenophyta

Fig. 2. Phytoplankton composition in Lake Bninskie from July to October in the years 2004–2007.

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Fig. 4. Phytoplankton composition in Lake Bytynskie from July to October in the years 2004–2007.

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Chlorophyta, Bacillariophyceae and other algalgroups were less abundant, never dominating thecommunities. Higher concentrations of algae otherthan cyanobacteria were observed only in 2005when the total phytoplankton biomass was thelowest over the study period. During the beginningof the sampling period, there was an increased totalbiomass of Chlorophyta and Dinophyta in LakeBN and of Chlorophyta and Cryptophyta inLake BY. Similarly in 2007, Chlorophyta andCryptophyta were relatively common in LakeBN. The dominant species were Coelastrum micro-porumNag. in A. Braun, Oocystis lacustris Chodat,Scenedesmus ecornis (Ehr. ex Ralfs) Chodat,Monoraphidium griffithii (Berk.) Kom.-Legn.(Chlorophyta), Cryptomonas erosa Ehrenberg,Cryptomonas reflexa (M. Marsson.) Skuja,Cryptopmonas marsonii Skuja, Rhodomonasminuta Skuja (Cryptophyta) and Peridiniopsis ber-olinense (Lemm.) Bourrelly (Dinophyta).The biomass of C. raciborskii in Lake BY was

generally slightly higher than in Lake BN duringthe period studied, with the exception of 2007. Thehighest concentration of C. raciborskii in bothlakes occurred in 2006 (Figs 2–5) but the highestcontribution of C. raciborskii to the total phyto-plankton biomass was in 2005 when it contributed18.5% of the total biomass in Lake BN and 9.3%in Lake BY.In Lake BN, the eigenvalues of the first two CCA

axes were 0.399 and 0.338 and significant (P50.05,Table 2). The first two CCA axes jointly explained31.8% of the total variance (2.00) in the phyto-plankton communities. The species–environmentcorrelations for CCA axes were relatively high, indi-cating a strong relationship between phytoplanktonand the environmental variables. Secchi depth, chla, and the TN/TP ratio were the most significantcontributors to CCA axis 1 (Fig. 6). CCA axis 2was most strongly correlated with PO3�

4 concentra-tions, temperature and water pH.

In Lake BY the eigenvalues of the first two CCAaxes were 0.462 and 0.208 and significant (P50.05,Table 2). The first two axes jointly explained35.2% of the total variance (1.53) in the commu-nities. The species-environment correlations forCCA axes were also high in Lake BY, indicatinga relatively strong relationship between phyto-plankton and the environmental variables. Secchidepth, pH, chl a, and the amount of total nutrientswere the most significant contributors to CCA axis1, with PO3�

4 , chl a and TN/TP ratio contributingmost to CCA axis 2 (Fig. 7).According to multiple regression analyses, bio-

mass of P. agardhii was significantly (P50.001)negatively related to Secchi depth in Lake BN(Table 3). In Lake BN, C. raciborskii was notrelated to any of the measured environmental var-iables. In Lake BY P. agardhii was significantly

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Fig. 5. Biomass of Planktothrix agardhii and Cylindrospermopsis raciborskii in Lake Bytynskie from July to October in theyears 2004–2007.

Table 2. The results of Canonical CorrespondenceAnalyses (CCA) with forward selected variables (P50.05)for Lake Bninskie (BN) and Lake Bytynskie (BY).

Lake BN Lake BY

Axis 1 Axis 2 Axis 1 Axis 2

Eigenvalue 0.399 0.338 0.462 0.208

Species-environment

correlation

0.890 0.935 0.963 0.762

Cumulative

percentage variance

of species data

17.2 31.8 24.3 35.2

Inter-set correlations

with axes

Temperature �0.060 0.390 0.345 �0.002

pH �0.044 �0.335 �0.727 0.122

SD �0.817 0.153 0.767 0.077

PO3�4 �0.218 �0.730 �0.028 0.323

NHþ4 0.216 0.235 0.590 �0.142

NO�3 �0.357 �0.241 0.586 �0.121

TP �0.154 �0.186 0.626 �0.096

TN 0.147 �0.255 0.667 �0.135

TN:TP 0.379 �0.007 �0.015 �0.160

Chl a 0.559 �0.112 �0.700 �0.219

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(P50.001) positively related to PO3�4 , chl a and

TP; and negatively related to Secchi depth, NO�3 ,and TN. C. raciborskii was also significantly(P50.001) positively related to NHþ4 .According to the Spearman correlation analysis,

P. agardhii was significantly negatively correlated(r¼ 0.149, p50.05) with C. raciborskii in Lake BN.Planktothrix agardhii was significantly negativelycorrelated (r¼ 0.438, P50.05) with C. raciborskiiin Lake BY. In addition, P. agardhii was signifi-cantly negatively correlated (r¼ 0.942, P50.05)with Shannon–Wiener diversity in Lake BN andin Lake BY (r¼ 0.781, P50.05).Cylindrospermopsis raciborskii was significantlypositively correlated (r¼ 0.542) with Shannon–Wiener diversity in Lake BY. In Lake BN, the cor-relation of C. raciborskii with Shannon–Wienerdiversity was non-significant (r¼ 0.208).

Discussion

Oscillatoriales dominated the phytoplankton com-munities in both lakes. Although communitieswere strongly dominated by P. agardhii, L. redekeiwas also abundant, thus supporting findings byRucker et al. (1997) that both species are oftenpresent in shallow and eutrophic waters, and com-pete successfully with other filamentous cyanobac-teria since they tolerate very low light conditions.In addition to the Oscillatoriales, Nostocales such

as Aphanizomenon flos-aquae, Aphanizomenongracile and C. raciborskii were relatively abundant.Cylindrospermopsis raciborskii was often presentand its abundance increased slightly after 2003(Stefaniak & Kokocinski, 2005). Its increasedabundance is typical for many eutrophic temperatelakes (Nixdorf et al., 2003; Stuken et al., 2006).Cylindrospermopsis raciborskii reached its highestbiomass during 2005, but biomass was nonethelessrelatively low in comparison with other groups ofalgae.The CCA indicated that turnover of the phyto-

plankton composition was controlled moststrongly by changes in Secchi depth (suggestingdifferences in light intensity), water temperature,water pH and nutrient concentrations. The resultsare highly congruent with other studies where theimportance of nutrient concentrations, tempera-ture and light has been documented (Forsstromet al., 2005; Grover & Chrzanowski, 2006;Kokocinski & Soininen, 2008). Although P. agard-hii and C. raciborskii often co-occurred, multipleregression analyses confirmed that these speciesresponded differently to several environmental var-iables. For example, the importance of light inten-sity for regulating P. agardhii was supported giventhat Secchi depth was a significant explanatoryvariable of its biomass in both lakes.More specifically, the biomass of P. agardhii wasnegatively related to Secchi depth supporting

Aphanizomenon flos-aquae

Aphanizomenongracile

Cylindrospermopsisraciborskii

Limnothrixredekei

Planktothrixagardhii

Pseudanabaena limnetica

Cryptomonaserosa

Cryptomonasmarssonii

Cryptomonasreflexa

Ceratium hirundinellaTemp

pH

SD

PO4

NH4

NO3 Tot P Tot N

N/P

Chl-a 11–3–

–1

1

Axis 1

Axi

s 2

Fig. 6. Ordination diagram for Canonical Correspondence Analysis of the phytoplankton assemblages in Lake Bninskie.

M. Kokocinski et al. 370

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earlier findings that it is able to grow exceedinglywell under low light intensities (Rucker et al., 1997;Scheffer et al., 1997; Nixdorf et al., 2003).Moreover, the finding that the biomass ofC. raciborskii was not related to Secchi depth wascongruent with our initial expectation that C. raci-borskii can grow under different light intensitiesand at high temperature (Fig. 1). Our findingsalso concur with Briand et al. (2004) since therewere no significant differences in growth rates ofC. raciborskii at different light intensities.

Both species preferred nutrient-rich waters, withP. agardhii being positively related to TP and PO3�

4

concentrations (in Lake BY), and C. raciborskii toNHþ4 concentrations. The fact that C. raciborskiiwas not related to phosphorus may suggest that ithas a high uptake and high storage capacity forphosphorus allowing it to grow under relativelylow phosphate supply (Branco & Senna, 1994;Presing et al., 1996; Isvanovics et al., 2000;Briand et al., 2002b). Recent experimental studiesalso showed that C. raciborskii is able to grow

Fragilaria ulna

Aphanizomenon gracile

Aphanizomenonissatschenkoi

Cylindrospermopsis raciborskii

Limnothrixredekei

Planktothrixagardhii

Pseudanabaena limnetica

Botryococcus braunii

Cryptomonas reflexa

Peridinium elpatiewskii

TemppH

SD

PO4

NH4

NO3

Tot PTot NN/PChl-a–2 2

Axis 1

Axi

s 2

Fig. 7. Ordination diagram for Canonical Correspondence Analysis of the phytoplankton assemblages in Lake Bytynskie.

Table 3. The results of multiple regression analyses for Lake Bninskie (BN) and Lake Bytynskie (BY) showing the main

environmental factors related to the abundance of P. agardhii and C. raciborskii.

Model R2 P

Lake BN

Planktothrix agardhii Y¼ 54.81� 64.6 � SD 0.517 0.000

Cylindrospermopsis raciborskii No significant variables in the model

Lake BY

Planktothrix agardhii Y¼ 54.16� 50.6 � SD� 0.04 �NO�3 þ 0.088 �PO3�4 þ 0.119 �Chla-a� 0.007 �TNþ 0.032 �TP 0.918 0.000

Cylindrospermopsis raciborskii Y¼ 0.122þ 0.003 �NHþ4 0.318 0.001

Ecology of Cylindrospermopsis raciborskii in two hypereutrophic lakes 371

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faster and sustain a high biomass under phospho-rus limitation during a sufficient supply of NHþ4 orNO�3 (Kenesi et al., 2009). In addition, NHþ4 wasshown to be effectively assimilated by C. racibors-kii in previous experimental studies by Spro

00

beret al. (2003). A positive relationship betweenC. raciborskii and NHþ4 in our study seems to sup-port these findings. In contrast, the growth ofP. agardhii is favoured by higher concentrationsof phosphorus and its dominance is especiallymarked in shallow, turbid lakes with intensiveinteraction between the sediment and watercolumn (Nixdorf et al., 2003; Noges & Jensen,2003).The different environmental requirements of

C. raciborskii and P. agardhii were indicated by theregression analyses where their abundances had anegative relationship. At low light intensities andlow temperature P. agardhii dominated the com-munity, whereas C. raciborskii was favoured byhigher temperatures and greater light intensities.The latter was evident, however, only in CCAwhere C. raciborskii was positively related toSecchi depth and water temperature. These find-ings are congruent with our initial predictions(Fig. 1). The finding that P. agardhii grows bestin turbid waters is also in agreement with studies byNixdorf et al. (2003) who place P. agardhii in thephytoplankton functional group S1 (sensuReynoldset al., 2002) of photoadapting filamentous cyano-bacteria common in shallow, wind-exposed lakeswith reduced light availability and intense sedi-ment–water interactions. Although C. raciborskiinever reached dominance, it increased in abundancewhen P. agardhii was less abundant.It is feasible that in this situation C. raciborskii

was able to out-compete P. agardhii, and theincreasing number of successful invasions byC. raciborskii in temperate regions supports thisview. This finding supports the hypothesis ofReynolds et al. (2002) that P. agardhii and C. raci-borskii belong to different functional groups.According to Padisak & Reynolds (1998) andReynolds et al. (2002) C. raciborskii has been allo-cated to the SN phytoplankton functional groupcharacteristic of warm, mixed waters enrichedwith phosphorus. The Shannon–Wiener diversitywas also consistently low when there was a highbiomass of P. agardhii. In contrast, C. raciborskiiwas positively correlated with Shannon–Wienerdiversity in Lake BY. These results indicate thatP. agardhii can be considered as a steady-state spe-cies during the Oscillatoriaceae-dominated steadystate in shallow lakes (Dokulil & Teubner, 2000;Scheffer et al., 1997; Scheffer, 1998) when few spe-cies are able to coexist (Nixdorf et al., 2003).To conclude, the abundances of P. agardhii and

the invasive C. raciborskii are negatively related,

possibly because they have different environmentalniches. As we initially predicted, P. agardhii isfavoured by turbid conditions with elevated phos-phorus concentrations, while the abundance ofC. raciborskii is directly related to ammoniumnitrogen and it prefers less turbid warmer waters.Our results may therefore shed more light onmechanisms promoting the invasion of C. racibors-kii in temperate regions. Future studies are neededto examine if C. raciborskii is able to sustain largepopulations in temperate lakes and to out-competethe native cyanobacteria.

Acknowledgements

Financial support was provided by the PolishMinistry of Science and Higher Education throughresearch grant No. N 304 051 31/1855 and by theAcademy of Finland and Kone foundation (to JS).We thank Dr Harold G. Marshall for his Englishlanguage revision and helpful comments on themanuscript.

References

BERGER, C. (1975). Occurrence of Oscillatoria agardhii Gom. in

some shallow eutrophic lakes. Verh. Internat. Verein. Limnol.,

19: 2689–2697.

BERGER, C. (1989). In situ primary production, biomass and light

regime in the Wolderwijd, the most stable Oscillatoria agardhii

lake in the Netherlands. Hydrobiologia, 188: 233–344.

BERTNESS, M.D. (1984). Habitat and community modification by

an introduced herbivorous snail. Ecology, 65: 370–381.

BOUVY, M., MOLICA, R., DE, OLIVEIRA, S., MARINHO, M. &

BEKER, B. (1999). Dynamics of a toxic cyanobacterial bloom

(Cylindrospermopsis raciborskii) in a shallow reservoir in the

semi-arid region of northern Brazil. Aquat. Microb. Ecol., 20:

285–297.

BRANCO, C.W.C. & SENNA, P.A.C. (1994). Factors influencing the

development of Cylindrospermopsis raciborskii and Microcystis

aeruginosa in the Paranoa Reservoir, Brasilia, Brazil. Algol.

Stud., 75: 85–96.

BRIAND, J.F., ROBILLOT, C., QUIBLIER-LLOBERAS, C. & BERNARD, C.

(2002a). A perennial bloom of Planktothrix agardhii

(Cyanobacteria) in a shallow eutrophic French lake: limnological

and microcystin production studies. Arch. Hydrobiol., 153:

605–622.

BRIAND, J.F., ROBILLOT, C., QUIBLIER-LIOBERAS, C., HUMBERT, J.F.,

COUTE, A. & BERNARD, C. (2002b). Environmental context of

Cylindrospermopsis raciborskii (Cyanobacteria) blooms in shal-

low pond in France. Water Res., 36: 3183–3192.

BRIAND, J.F., LEBOULANGER, C., HUMBERT, J.F., BERNARD, C. &

DUFOUR, P. (2004). Cylindrospermopsis raciborskii

(Cyanobacteria) invasion at mid-latitudes: selection, wide phy-

siological tolerance, or global warming? J. Phycol., 40: 231–238.

CASTRO, D., VERA, D., LAGOS, N., GARCIA, C. & VASQUEZ, M.

(2004). The effect of temperature on growth and production of

paralytic shellfish poisoning toxins by the cyanobacterium

Cylindrospermopsis raciborskii C10. Toxicon, 44: 483–489.

CARMICHAEL, W.W. (1994). The toxins of Cyanobacteria. Sci. Am.,

270: 64–70.

CHONUDOMKUL, D., YONGMANITCHAI, W., THEERAGOOL, G.,

KAWACHI, M., KASAI, F., KAYA, K. & WATANABE, M.M.

(2004). Morphology, genetic diversity, temperature tolerance

and toxicity of Cylindrospermopsis raciborskii (Nostocales,

M. Kokocinski et al. 372

Downloaded By: [Kokocinski, Mikolaj] At: 19:47 21 September 2010

Cyanobacteria) strains from Thailand and Japan. FEMS

Microbiol. Ecol., 48: 345–355.

CHORUS, I. (2001). Cyanotoxins: Occurrence, Causes, Consequences.

Springer-Verlag KG, Berlin.

CROSSETTI, L.O. & DE M. BICUDO, C. (2008). Adaptations in phy-

toplankton life strategies to imposed change in a shallow urban

tropical eutrophic reservoir, Garcas Reservoir, over 8 years.

Hydrobiologia, 614: 91–105.

DE SOUZA, R.C.R., CARVALHO, M.C. & TRUZZI, A.C. (1998).

Cylindrospermopsis raciborskii (Wolosz.) Seenaya and Subba

Raju (Cyanophyceae) dominance and a contribution to the

knowledge of Rio Pequeno arm, Billings Reservoir, Brazil.

Environ. Toxicol. Water Qual., 13: 73–81.

DOKULIL, M.T. & MAYER, J. (1996). Population dynamics and

photosynthetic rates of a Cylindrospermopsis–Limnothrix asso-

ciation in highly eutrophic urban lake, Alte Donau, Austria.

Algol. Stud., 83: 179–195.

DOKULIL, M.T. & TEUBNER, K. (2000). Cyanobacterial dominance

in lakes. Hydrobiologia, 438: 1–12.

DUKES, J.S. & MOONEY, H.A. (1999). Does global change increase

the success of biological invaders? Trends Ecol. Evol., 14:

135–139.

FONSECA, B.M. & DE M. BICUDO, C.E. (2008). Phytoplankton sea-

sonal variation in a shallow stratified eutrophic reservoir (Garcas

Pond, Brazil). Hydrobiologia, 600: 267–282.

FORSSTROM, L., SORVARI, S. & KORHOLA, A. (2005). Seasonality of

phytoplankton in subarctic Lake Saanajarvi in NW Finnish

Lapland. Polar Biol., 28: 846–861.

FRIDRIKSSON, S. & MAGNUSSON, B. (1992). Development of the

ecosystem on Surtsey with references to Anak Krakatau.

GeoJournal, 28: 287–291.

GEORGE, D.G., TALLING, J.F. & RIGG, E. (2000). Factors influen-

cing the temporal coherence of five lakes in the English Lake

District. Freshwat. Biol., 43: 449–461.

GERTEN, D. & ADRIAN, R. (2000). Climate-driven changes in spring

plankton dynamics and the sensitivity of shallow polymictic lakes

to the North Atlantic Oscillation. Limnol. Oceanogr., 45:

1058–1066.

GROVER, J.P. & CHRZANOWSKI, T.H. (2006). Seasonal dynamics of

phytoplankton in two warm temperate reservoirs: association of

taxonomic composition with temperature. J. Plankton Res., 28:

1–17.

HINDAK, F., editor (1978). Freshwater Algae. Slovenske

Pedagogicke Nakladelstvo, Bratislava.

ISVANOVICS, V., SHAFIK, H.M., PRESING, M. & JUHOS, S. (2000).

Growth and phosphate uptake kinetics of the cyanobacterium,

Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow

cultures. Freshwat. Biol., 2: 257–275.

JAVORNICKY, P. (1958). Revise nekterych method pro

zjist’ovanıkvantity fitoplantonu (Revision of some methods for

the phytoplankton quantity estimation). Scientific Paper 2,

Faculty of Technology of Fuel and Water, Institute of

Chemical Technology, Prague, pp. 283–267.

KENESI, G., SHAFIK, H.M., KOVACS, A.W., HERODEK, S. &

PRESING, M. (2009). Effect of nitrogen forms on growth, cell

composition and N2 fixation of Cylindrospermopsis raciborskii

in phosphorus-limited chemostat cultures. Hydrobiologia, 623:

191–202.

KOKOCINSKI, M., DZIGA, D., SPOOF, L., STEFANIAK, K., JURCZAK, T.,

MANKIEWICZ-BOCZEK, J. & MERILUOTO, J. (2009). First report of

the cyanobacterial toxin cylindrospermopsin in the shallow,

eutrophic lakes of western Poland. Chemosphere, 74: 669–675.

KOKOCINSKI, M. & SOININEN, J. (2008). Temporal variation in phy-

toplankton in two lakes with contrasting disturbance regimes.

Fundam. Appl. Limnol., 171: 39–48.

LAGOS, N., ONODERA, H., ZAGATTO, P.A., ANDRINOLO, D.,

AZEVEDO, S.M.F.Q. & OSHIMA, Y. (1999). The first evidence of

paralytic shellfish toxins in the freshwater cyanobacterium

Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon,

37: 1359–1373.

LEGENDRE, P. & LEGENDRE, L. (1998). Numerical ecology. 2nd

English ed. Elsevier Science BV, Amsterdam.

LI, R., CARMICHAEL, W.W., BRITTAIN, S., EAGLESHAM, G.K.,

SHAW, G.R., NOPARATNARAPORN, A.M.N., YONGMANITCHAI, W.,

KAYA, K. & WATANABE, M.M. (2001). Detection of

cylindrospermopsin from a strain of Cylindrospermopsis

raciborskii (Cyanobacteria) isolated from Thailand. Toxicon,

39: 973–980.

MACK, R.N., SIMBERLOFF, D., LONSDALE, W.M., EVANS, H.,

CLOUT, M. & BAZZAZ, F.A. (2000). Biotic invasions: causes, epi-

demiology, global consequences and control. Ecol. Appl., 10:

689–710.

MANTI, G., MATTEI, D., MESSINEO, V., MELCHIORRE, S.,

BOGIALLI, S., SECHI, N., CASIDDU, P., LUGLIO, L., DI BRIZIO, M.

& BRUNO, M. (2005). First report of Cylindrospermopsis racibors-

kii (Nostocales, Cyanophyta) in Italy. Harmful Algae News, 28:

8–9.

MISCHKE, U. & NIXDORF, B. (2003). Equilibrium phase

conditions in shallow German lakes: how Cyanoprocaryota

species establish a steady state phase in late summer.

Hydrobiologia, 502: 123–132.

NICKLISCH, A., SHATWELL, T. & KOHLER, J. (2008). Analysis and

modelling of the interactive effects of temperature and light on

phytoplankton growth and relevance for the spring bloom.

J. Plankton Res., 30: 75–91.

NIXDORF, B. (1994). Polymixis of a shallow lake (Großer

Muggelsee, Berlin) and its influence on seasonal phytoplankton

dynamics. Hydrobiologia, 275/276: 173–186.

NIXDORF, B., MISCHKE, U. & RUCKER, J. (2003). Phytoplankton

assemblages and steady state in deep and shallow eutrophic

lakes – an approach to differentiate the habitat properties of

Oscillatoriales. Hydrobiologia, 502: 111–121.

NO00

GES, P. & JENSEN, J.P. (2003). Occurrence, coexistence and

competition of Limnothrix redekei and Planktothrix agardhii:

analysis of Danish–Estonian lake database. Algol. Stud., 109

(Cyanobacterial Research 4): 429–441.

OHTANI, I., MOORE, R.E. & RUNNEGAR, M.T.C. (1992).

Cylindrospermopsin: a potent hepatotoxin from the blue-green

alga Cylindrospermopsis raciborskii. J. Am. Chem. Soc., 114:

7941–7942.

OTT, I., NOGES, P., LAUGASTE, R. & KOIV, T. (2003). Occurrence of

Limnothrix redekei Van Goor in Estonian lakes. Algol. Stud., 109

(Cyanobacterial Research 4): 455–468.

PADISAK, J. (1997). Cylindrospermopsis raciborskii (Woloszynska)

Seenayya et Subba Raju, an expanding, highly adaptative cya-

nobacterium: worldwide distribution and review of its ecology.

Arch. Hydrobiol., Suppl., 107: 563–593.

PADISAK, J. & REYNOLDS, C.S. (1998). Selection of phytoplankton

associations in Lake Balaton, Hungary, in response to eutrophi-

cation and restoration measures, with special reference to the

cyanoprokaryotes. Hydrobiologia, 384: 41–53.

PAERL, H.W. & HUISMAN, J. (2008). Blooms like it hot. Science,

320: 57–58.

PELECHATA, A., PELECHATY, M. & PUKACZ, A. (2006).

Cyanoprokaryota of shallow lakes of Lubuskie Lakeland (mid-

western Poland). Ocean. Hydrob. Stud., 35: 3–14.

POST, A., DE WIT, R. & MUR, L.R. (1985). Interactions between

temperature and light intensity on growth and photosynthesis of

the cyanobacterium Oscillatoria agardhii. J. Plankton Res, 7:

487–495.

POULICKOVA, A., HASLER, P. & KITNER, M. (2004). Annual

cycle of Planktothrix agardhii (Gommont) Anagnostidis &

Komarek nature population. Int. Rev. Hydrobiol, 89:

278–288.

PRESING, M., HERODEK, S., VOROS, L. & KOBOR, I. (1996). Nitrogen

fixation, ammonium and nitrate uptake during a bloom of

Cylindrospermopsis raciborskii in Lake Balaton. Arch.

Hydrobiol, 136: 553–562.

RAMBERG, L. (1988). Relations between planktic blue-green algal

dynamics and environmental factors in four eutrophic Swedish

lakes. Arch. Hydrobiol, 112: 161–175.

REYNOLDS, C.S., HUSZAR, V., KRUK, C., NASELLI-FLORES, L. &

MELO, S. (2002). Towards a functional classification of the fresh-

water phytoplankton. J. Plankton Res., 24: 417–428.

Ecology of Cylindrospermopsis raciborskii in two hypereutrophic lakes 373

Downloaded By: [Kokocinski, Mikolaj] At: 19:47 21 September 2010

ROMO, S. & MIRACLE, M.R. (1993). Long-term periodicity of

Planktothrix agardhii, Pseudanabaena galeata and Geitlerinema

sp. in a shallow hypertrophic lagoon, the Albufera of Valencia

(Spain). Arch. Hydrobiol., 126: 469–486.

ROMO, S. & MIRACLE, M.R. (1994). Long-term phytoplankton

changes in a shallow hypertrophic lake, Albufera of Valencia

(Spain). Hydrobiologia, 275: 153–164.

RUCKER, J., WIEDNER, C. & ZIPPEL, P. (1997). Factors controlling

the dominance of Planktothrix agardhii and Limnothrix redekei

in eutrophic shallow lakes. Hydrobiologia, 342/343: 107–115.

SAKER, M.L. & GRIFFITHS, D.J. (2000). The effect of temperature

on growth and cylindrospermopsin content of seven isolates of

the cyanobacterium Cylindrospermopsis raciborskii

(Woloszynska) Seenayya and Subba Raju from water bodies in

northern Australia. Phycologia, 39: 349–354.

SAKER, M.L., NOGUEIRA, I.C.G., VASCONCELOS, V.M.,

NEILAN, B.A., EAGLESHAM, G.K. & PEREIRA, P. (2003). First

report and toxicological assessment of the cyanobacterium

Cylindrospermopsis raciborskii from Portuguese freshwaters.

Ecotoxicol. Environ. Safety, 55: 243–250.

SCHEFFER, M. (1998). Ecology of Shallow Lakes. Chapman & Hall,

London.

SCHEFFER, M., RINALDI, S., GRAGNAMI, A., MUR, L.R. &

VAN NES, E.H. (1997). On the dominance of filamentous

Cyanobacteria in shallow, turbid lakes. Ecology, 78: 272–282.

SHANNON, C.E. (1948). A mathematical theory of communication.

Bell System Technical Journal, 27: 626–656.

SPRO00

BER, P., SHAFIK, M.H., PRESING, M., KOVACS, A.W. &

HERODEK, S. (2003). Nitrogen uptake and fixation in the cyano-

bacterium Cylindrospermopsis raciborskii under different nitro-

gen conditions. Hydrobiologia, 506–509: 169–174.

STEFANIAK, K. & KOKOCINSKI, M. (2005). Occurrence of invasive

Cyanobacteria species in polimictic lakes of the Wielkopolska

region (Western Poland). Ocean. Hydrob. Stud., 34, Suppl, 3:

137–148.

STUKEN, A., RUCKER, J., ENDRULAT, T., PREUSSEL, K., HEMM, M.,

NIXDORF, B., KARSTEN, U. & WIEDNER, C. (2006). Distribution of

three alien cyanobacterial species (Nostocales) in northeast

Germany: Cylindrospermopsis raciborskii, Anabaena bergii and

Aphanizomenon aphanizomenoides. Phycologia, 45: 696–703.

TER BRAAK, C.J.F. (1986). Canonical correspondence analysis: a

new eigenvector technique for multivariate direct gradient ana-

lysis. Ecology, 67: 1167–1178.

TER BRAAK, C.J.F. & SMILAUER, P. (1998). Program CANOCO,

version 4.0. Centre for Biometry, Wageningen.

VAN LIERE, L. & MUR, L.R. (1980). Occurrence of Oscillatoria

agardhii and some related species, a survey. In Developments in

Hydrobiology, Vol. 2 (Barica, J. & Mur, L.E., editors), 67–77. Dr.

W. Junk BV, The Hague.

VITOUSEK, P.M. (1990). Biological invasions and ecosystem pro-

cess – towards an integration of population biology and ecosys-

tem studies. Oikos, 57: 7–13.

WALTHER, G.-R. (2003). Plants in a warmer world. Perspect. Plant

Ecol. Evol. System., 6: 169–185.

WELLS, M.J., POYNTON, A.A., BALSINHAS, K.J., MUSIL, H., VAN

HOEPEN, J.E. & ABBOTT, S.K. (1986). The history of introduction

of invasive alien plants to southern Africa. In The Ecology and

Management of Biological Invasions in Southern Africa

(Macdonald, A.W., Kruger, F.J. & Ferrar, A.A., editors),

21–35. Oxford University Press, Cape Town.

WETZEL, R.G. & LIKENS, G.F. (2000). Limnological Analyses. 3rd

ed. Springer-Verlag, New York.

WIEDNER, C., NIXDORF, B., HEINZE, R., WIRSING, B., NEUMANN, U.

& WECKESSER, J. (2002). Regulation of Cyanobacteria and micro-

cystin dynamics in polymictic shallow lakes. Arch. Hydrobiol.,

155: 383–400.

WIEDNER, C., RUCKER, J., BRUGGEMANN, R. & NIXDORF, B. (2007).

Climate change affects timing and size of populations of inva-

sive cyanobacterium in temperate regions. Oecologia, 152:

473–484.

M. Kokocinski et al. 374

Downloaded By: [Kokocinski, Mikolaj] At: 19:47 21 September 2010