Abstract The phytoplankton species composi-

tion and seasonal succession were examined in

Lake Kastoria during the period November 1998–

October 1999. A total of 67 species and 19 func-

tional groups were identified. Only 4 out of the 67

species, all Cyanobacteria, were dominant (Lim-

nothrix redekei, Microcystis aeruginosa, Cylindro-

spermopsis raciborskii and Aphanizomenon

gracile). Diatoms were rare, not only in terms of

species number, but also in terms of biomass

(contributing < 5% to the total phytoplankton

biomass) in relation to the rather low silicon con-

centrations throughout the year. The functional

groups S1, SN, M and H1 were found dominant in

the lake. The species A. gracile (functional group

H1) behaved like the species Cylindrospermopsis

raciborskii(functional group SN) which is tolerant

to mixing and poor light conditions. The phyto-

plankton seasonal succession showed similar pat-

terns in all six sampling stations, both at the surface

and the bottom water layer, with minor differences

during Microcystis aeruginosa dominance. Two

steady-state phases were identified within a year

lasting for 4 months under relatively stable physi-

cal conditions. In these steady-states, the Limno-

thrix redekei persistent dominance under low light

availability and low inorganic nitrogen has been

explained by its specific ability such as buoyancy

regulation to exploit resources in the water col-

umn. Moreover, high population densities over the

winter and before the development of daphnids

may contribute to the steady-state dominance of

Limnothrix. Different niches separated vertically

in the water column is one of the explanations for

the Limnothrix–Microcystis steady-state when a

replacement between the two species was observed

in different water layers and areas of the lake. Long

lasting steady-states of Cyanobacteria observed in

Lake Kastoria and in other Mediterranean and

tropical freshwaters may indicate influence of warm

climate properties on phytoplankton dynamics.

Handling editor: K. Martens

Electronic Supplementary Material Supplementarymaterial is available to authorized users in the onlineversion of this article at http://dx.doi.org/10.1007/s10750-006-0360-4

M. Moustaka-Gouni (&)Department of Botany, School of Biology, AristotleUniversity of Thessaloniki, GR-541 24 Thessaloniki,Greecee-mail: mmustaka@bio.auth.gr

Present Address:E. VardakaDepartment of Fisheries and AquacultureTechnology, Alexander Technological EducationalInstitute of Thessaloniki, Campus of Nea Moudania,P.O. Box 157, GR-632 00 Nea Moudania, Greece

Present Address:E. TryfonAdministration of Environmental Planning, HellenicMinistry for the Environment, Physical Planning andPublic Works, GR-112 51 Athens, Greece

Hydrobiologia (2007) 575:129–140

DOI 10.1007/s10750-006-0360-4

123

PRIMARY RESEARCH PAPER

Phytoplankton species succession in a shallowMediterranean lake (L. Kastoria, Greece): steady-statedominance of Limnothrix redekei, Microcystis aeruginosaand Cylindrospermopsis raciborskii

Maria Moustaka-Gouni Æ Elisabeth Vardaka ÆEleni Tryfon

Received: 29 March 2006 / Revised: 4 July 2006 / Accepted: 8 July 2006 / Published online: 25 September 2006� Springer Science+Business Media B.V. 2006

Keywords Phytoplankton succession ÆFunctional groups Æ Cyanobacteria

steady-states Æ Polymictic Mediterranean lake

Introduction

Phytoplankton dynamics has been the subject of

many studies in freshwaters but only in a few

cases it is examined in relation to equilibrium/

non-equilibrium theories (e.g. Salmaso, 2003).

For identification of equilibrium states in phyto-

plankton seasonal succession, Sommer et al.

(1993) set three criteria: (i) a maximum of three

species of algae contribute more than 80% of total

biomass, (ii) their dominance persists for more than

1–2 weeks and (iii) during that period the total

biomass does not increase significantly. Recent

studies dealing with ‘‘equilibrial’’ species and

assemblages clarify our understanding of steady-

states in phytoplankton succession in a wide spec-

trum of freshwaters, mostly from mid-latitudes

(Naselli-Flores et al., 2003). Different types of

phytoplankton steady-states have been explained

as the result not necessarily of competition but due

to several other processes (e.g. grazing, species

specific abilities; Albay & Akcaalan, 2003; Rojo &

Alvarez-Cobelas, 2003).

Steady-state phases are rarely attained in phy-

toplankton succession. However they have been

observed more regularly in shallow hypertrophic

lakes where Cyanobacteria are primarily the pro-

tagonists (Mischke & Nixdorf, 2003; Nixdorf et al.,

2003). A Limnothrix redekei steady-state assem-

blage has been reported so far only in one case

(Rojo & Alvarez Cobelas, 2003). L. redekei, a

typical phytoplankter in turbid mixed layers

(Reynolds et al., 2002) of lakes and lowland rivers

of central and northern Europe (Meffert, 1989), is

not common in southern Europe (Gkelis et al.,

2005). In contrast, Cylindrospermopsis raciborskii

is a low-latitude species known for its invasive

behavior in mid-latitudes (Padisak, 1997). C. rac-

iborskii, Aphanizomenon gracile and Microcystis

aeruginosa have been found dominant in summer

steady-state assemblages of hypertrophic shallow

wetlands in southern Europe (Stoyneva, 2003).

In this work, we examine the seasonal succes-

sion of phytoplankton during an annual study in

Lake Kastoria, a highly eutrophic shallow lake.

The phytoplankton species are classified accord-

ing to functional groups proposed by Reynolds

et al. (2002) and Padisak et al. (2003). When

examining succession, we try to identify steady-

state phases and to understand the environmental

factors that promote, maintain and disturb the

dominant species in these phases. This investiga-

tion on a relatively large shallow lake in the

Mediterranean region will contribute to the lim-

ited knowledge of the compositional diversity of

dominants in steady-state phases of shallow lakes,

the frequency and longevity of the phases. More-

over, the study of Cyanobacteria steady-states

may have application in the much needed mea-

sures to restore water quality in eutrophic lakes.

Study site

Lake Kastoria (Fig. 1) is situated at latitude

40�30¢ N, and longitude 21�18¢ E in Northern

Greece. It covers 24 km2, has a maximum depth

of 8 m, an average depth of 4 m and a water

retention time greater than 2 years. The lake’s

outflow discharge is man controlled through

manipulation of the water level when it reaches

its maximum. A substantial water inflow increase

during January–March 1999 caused the lake to

overflow and the local authorities discharged

NN

S6

S5

S4

S3

S2

S1

40° 30' N

21° 18' E

1 km1 km

3 m5 m7 m

Fig. 1 Map of Lake Kastoria showing the six samplingstations (S1, S2, S3, S4, S5, S6) and the depth contours (3 m,5 m, 7 m) in the lake. Insert, map of Greece (solid squareindicates the position of Lake Kastoria)

130 Hydrobiologia (2007) 575:129–140

123

large amounts of water in the spring of that year

in order to control the water level.

Human impact on the lake and its catchment

was diverse. Hydraulic adjustments, fish stock

management with the introduction of cyprinoids

and macrophyte cutting are just some among

them. Moreover, Kastoria is an urban lake that

had been receiving sewage effluents for decades

until 1995. Former studies of Lake Kastoria have

been made that show among other things high

concentrations of inorganic nitrogen and phos-

phorus (Moustaka-Gouni et al., 2006). Never-

theless, there are periods when inorganic nitrogen

and phosphorus fall below the threshold values

used to detect N and P limitation (Reynolds et al.,

2002). Dissolved silicon never exceeded

15 lmol l–1 in the lake water (Table 1). The peak

values of planktic Cyanobacteria biomass indicate

a highly eutrophic system (Vardaka et al., 2000)

that has a history of toxic cyanobacterial blooms

(Lanaras et al., 1989; Cook et al., 2004). Possible

effects of toxic cyanobacterial blooms on hetero-

trophic nanoplankton, both positive and negative,

and a weak structure of microbial food web in the

lake, have recently been reported (Moustaka-

Gouni et al., 2006).

Methods

Sampling was carried out from November 1998 to

October 1999 fortnightly during the warm period

of the year and monthly during the cold period.

Ice cover on the lake, thin in some periods, pro-

hibited sampling in December 1998. Water sam-

ples were collected from six stations in the deeper

area of the lake’s basin (S1, S2, S3, S4, S5, S6;

Fig. 1). The samples were collected from the

surface (0–1 m) and the bottom layer (one meter

above sediment varying from 4 m to 7 m at the

maximum depth).

The methods used for in situ measurements,

chemical analyses of nutrients and microscopical

analysis of phytoplankton have been described by

Moustaka-Gouni et al. (2006). Phytoplankton

counts (cells, filaments, colonies) were performed

using the inverted microscope method. To convert

colony counts of Microcystis aeruginosa to cell

numbers, the average number of cells of 30 colonies

was determined using the equation of Reynolds &

Jaworski (1978). Cell and filament volumes were

estimated from appropriate geometric formulae

after measuring the dimensions of 30 cells/fila-

ments.

The mixing zone (zmix) was identified using

temperature profiles and the euphotic zone (zeu)

calculated as 2.0 times the Secchi depth. An index

of light availability (LI) was calculated according

to Makulla & Sommer (1993):

LI ¼ 2ðSD=zmixÞ � ðD=24Þ

where LI is the light index, SD is Secchi depth

(m), zmix is mixing depth and D is daylength (h).

Phytoplankton functional groups were estab-

lished according to Reynolds et al. (2002) and

Padisak et al. (2003). Species were considered

dominant if they contributed more than 10% to the

total phytoplankton biomass in each individual

sampling date. Steady-state phases (SSI, SSII) were

identified when (i) 1, 2 or 3 phytoplankton species

contributed more than 80% to total biomass, (ii)

their existence or co-existence occurred for more

than 3 weeks and (iii) during that period the species

Table 1 Nutrient concentrations (min, max) during the whole study (November 1998–October 1999) and selected periodsof the year in Lake Kastoria (‘u.d.l.’ denotes ‘under detection limit’)

Nutrient concentration (lmol l–1) Nov 27–Oct 10 Jan 19–Mar 23 Jun 14–Aug 11 Aug 31–Oct 10

Min Max Min Max Min Max Min Max

PO4-P u.d.l. 1.0 0.2 0.4 0.1 0.6 0. 6 1.0Total P 1.7 17.7 1.7 2.0 3.9 16.3 3.9 5.8NO3-N 0.4 6.4 1.5 2.5 0.4 1.2 0. 7 1.2NO2-N u.d.l. 0.4 0.1 0.2 u.d.l. 0.2 u.d.l. 0.3NH4-N u.d.l. 8.8 0.4 1.4 u.d.l. 3.2 1.0 5.3Dissolved inorganic nitrogen 0.7 11.9 2.0 3.8 0.7 3.9 2.0 6.6SiO2-Si 9.2 14.7 10.4 11.4 9.7 13.4 9.2 14.7

Hydrobiologia (2007) 575:129–140 131

123

composition of the community was almost

unchanged and the total phytoplankton biomass

differed non-significantly (ANOVA, P > 0.05)

between sampling dates or less than 20% from that

of the previous sampling date value.

A one way ANOVA test was used to compare

the means of phytoplankton biomass among

sampling dates. A Pearson correlation analysis

was used to determine relationships between

biological variables. The relationship between the

biomass of dominant species and temperature was

analyzed using non-linear regression analysis.

Principal Component Analysis (PCA; Legendre

& Legendre, 1998) was used to examine the

relationship between physical and chemical

properties of the water and the relative domi-

nance of phytoplankton dominant species during

the period of their coexistence. In PCA analysis

and when necessary, log transformation of values

were made to achieve normality.

Results

Phytoplankton species composition

and biomass

A total of 67 phytoplankton species have been

identified (Table 2) in the water samples exam-

ined throughout the year. Chlorophytes contrib-

uted the highest number of species (29) followed

by Cyanobacteria (20), diatoms (5), dinophytes

(4), cryptophytes (3), euglenophytes (2), xantho-

phytes (2), chrysophytes (1) and prymnesiophytes

(1). The functional group J was the best repre-

sented in number of species followed by M and

H1 (Table 2).

Phytoplankton biomass consisted mainly of

Cyanobacteria (contributing 91.8% to the annual

mean biomass) (Fig. 2). Abrupt seasonal varia-

tions in total phytoplankton biomass with almost

constant contribution by different taxonomic

groups have been observed throughout the year.

Nevertheless, periods with rather constant species

composition and biomass have also been recog-

nized (phases SSI and SSII; Fig. 2).

Only 4 out of the 67 species were dominant

throughout the year. These species, all Cyano-

bacteria, belong to different functional groups of

phytoplankton: Limnothrix redekei to S1,

Cylindrospermopsis raciborskii to SN, Microcystis

aeruginosa to M and Aphanizomenon gracile to

H1. The species Aphanizomenon issatschenkoi

(H1), Ceratium hirundinella (LM), Cryptomonas

sp. (Y), Peridinium sp. (LO), Monoraphidium

griffithii (X1), Phacotus lenticularis (YPh) and

Nitzschia acicularis (D) contributed < 10% to the

total phytoplankton biomass. The nanoflagellates

Rhodomonas minuta (X2) and Chrysochromulina

parva (X2), although abundant, contributed < 5%

to the total phytoplankton biomass.

The four dominant species made up 91% of

mean total phytoplankton biomass influencing

significantly the temporal distribution of the total

phytoplankton biomass (r = 0.989, P < 0.001).

Limnothrix redekei persisted throughout the year

showing the highest biomass during the cold

period of the year (Fig. 3a). Cylindrospermopsis

raciborskii and Aphanizomenon gracile devel-

oped during the summer when the temperature

exceeded 20�C (Fig. 3b, c). Microcystis aerugin-

osa population increased from late summer to

autumn in the range of 17–27�C (Fig. 3d).

PCA was used to examine how dominant spe-

cies are grouped in relation to physical and

chemical parameters during the summer–autumn

period (Fig. 4) when all dominant species coex-

isted. The first two axes with the largest eigen-

values explain 37.7 and 29.5% of the total

variance in the data, respectively. Cylindro-

spermopsis highest dominance (>40%) is differ-

entiated along axis I by lower nitrate and

ammonia nitrogen concentrations, lower zmix:zeu

and N:LI ratios. Along axis II, Cylindrosperm-

opsis and Aphanizomenon dominance together

with Limnothrix is differentiated by higher tem-

peratures while Microcystis co-dominance with

Limnothrix is differentiated by higher phosphate

phosphorus concentrations, and higher zmix:zeu

and N:LI ratios.

Phytoplankton seasonal succession

Similar patterns of phytoplankton succession have

been observed in all six sampling stations both at

the surface and the bottom layers (Fig. 5). How-

ever, the spatial similarity in phytoplankton

dominance declined during August–October

132 Hydrobiologia (2007) 575:129–140

123

Table 2 List of taxa and functional groups identified in Lake Kastoria during November 1998–October 1999

Taxa Functional group

CyanobacteriaAphanocapsa elachista W. et G. S. West KAphanothece sp. KChroococcus limneticus Lemm.Merismopedia tenuissima Lemm.Microcystis aeruginosa (Kutz.) Kutz. MM. flos-aquae (Wittr.) Kirchn. MM. ichthyoblabe Kutz. MM. novacekii (Kom.) Comp. MM. wesenbergii (Kom.) Kom. In Kondr. MPannus spumosus HickelSnowella lacustris (Chod.) Kom. et Hind. LO

Synechococcus sp. ZWoronichinia naegeliana (Unger) Elenk. LO

Limnothrix redekei (Van Goor) Meffert S1Anabaena cf. aphanizomenoides Forti H1A. flos-aquae Breb ex Born et Flah. H1A. viguieri Denis et Fremy H1Aphanizomenon gracile (Lemm.) Lemm. (H1) SN

A. issatschenkoi (Usac) Prosk. – Lavr. H1Cylindrospermopsis raciborskii (Wolosz.) Seen. et Sub. Raju SN

ChlorophyceaeChlamydomonas sp.Phacotus lenticularis (Ehrenb.) SteinAnkistrodesmus sp.Botryococcus braunii Kutz. FCoelastrum microporum Nag. JC. astroideum De – Not. JDictyosphaerium pulchellum WoodLagerheimia sp.Monoraphidium cf. nanum (Ettl.) Hind. X1M. arcuatum (Kors.) Hind. X1M. griffithii (Berk.) Kom. – Legn. X1Nephrochlamys cf. willeana (Printz.) Kors.Oocystis sp. FPediastrum boryanum (Turp.) Menegh. JP. duplex Meyen JP. simplex Meyen JP. tetras (Ehrenb.) Ralfs JPseudodidymocystis fina (Kom.) Hege et DeasonScenedesmus acuminatus (Lagerh.) Chod. JScenedesmus sp. JSelenastrum sp.Tetraedron cf. triangulare Kors.T. caudatum (Corda) Hansg.T. minimum (A. Br.) Hansg.Tetrastrum staurogeniaeforme (Schrod.) Lemm.Elakatothrix genevensis (Reverd.) Hind.Closterium acutum Breb. PStaurastrum cf. chaetoceras (Schrod.) G. M. Smith PStaurastrum sp. P

EuglenophyceaeEuglena sp. W1Trachelomonas volvocinopsis Swir. W2

BacillariophyceaeCyclotella sp. C

Hydrobiologia (2007) 575:129–140 133

123

when Microcystis aeruginosa contributed >50% of

the total phytoplankton biomass in the sampling

stations S2 and S6. Two different types can be

recognized in the course of phytoplankton suc-

cession: (a) the mono-dominance of Limnothrix

redekei and (b) the co-dominance of (i) L. redekei–

Cylindrospermopsis raciborskii-Aphanizomenon

gracile and (ii) Limnothrix redekei–Microcystis

aeruginosa–Cylindrospermopsis raciborskii.

The mono-dominance of Limnothrix was

observed during both the high and low phyto-

plankton biomass periods (January–March and

May–June, respectively). The first period is

identified as a steady-state phase of phytoplank-

ton (SSI; Fig. 5). This species contributing >80%

to the total phytoplankton biomass persisted for

2 months, when composition and total biomass of

phytoplankton did not change considerably (see

Fig. 2). This steady-state phase was observed

almost identically in different areas and layers of

the lake (Fig. 5). The period of the steady-state

phase is characterized by low water temperature

(between 3.9 and 8.2�C) and low light availability

(LI ranged from 0.07 to 0.15) throughout the

isothermally mixed column (see Electronic Sup-

plementary Material). Nitrate and ammonia

nitrogen remained low ( < 2.5 lmol l–1and < 1.4

lmol –1, respectively) and phosphate phosphorus

ranged between 0.2 lmol l–1 and 0.4 lmol l–1,

(Table 1).

Over summer, three species of phytoplankton,

Limnothrix redekei, Cylindrospermopsis raciborskii

and Aphanizomenon gracile persisted for 2 months

but, since total phytoplankton biomass changed

considerably (see Fig. 2), no steady-state stage can

be recognized. This period is characterized by

Table 2 continued

Taxa Functional group

Aulacoseira granulata (Ehrenb.) Ralfs DStephanodiscus hantzschii Grun. DNitzschia acicularis W. Smith DSynedra sp. D

CryptophyceaeCryptomonas curvata Ehrenb. YCryptomonas sp. YRhodomonas minuta Skuja X2

DinophyceaeCeratium hirundinella (O. F. Muller) Schrank LM

Gymnodinium sp.Peridiniopsis elpatiewskyi (Ostenf.) Bourr. LO

Peridinium sp. LO

PrymnesiophyceaeChrysochromulina parva Lackey X2

XanthophyceaeGoniochloris sp.Pseudostaurastrum sp.

ChrysophyceaeMallomonas sp. E

Month

N D J F M A M I I A S O

Bio

mas

s (m

g l-1

)

0

1

10

20

30 CyanophytesChlorophytesDiatomsCryptophytesDinophytesPrymnesiophytes

SSI SSII

1998 1999

Fig. 2 Variations of the phytoplankton taxonomic groupsbiomass in Lake Kastoria during November 1998–October1999. Values are means and refer to the surface andbottom layers from all six stations. Periods of steady-statesare indicated as SSI and SSII

134 Hydrobiologia (2007) 575:129–140

123

intermittent thermal stratification (see Electronic

Supplementary Material) and high light availability

(LI up to 1.2; see Electronic Supplementary Mate-

rial). Low N:P (min. 1.4) and N:LI (min. 8.1) re-

source ratios (see Electronic Supplementary

Material) prevailed during the period of Cylindro-

spermopsis raciborskii and Aphanizomenon gracile

dominance.

A second steady-state phase (SSII; Fig. 5)

identified during the period August–October. The

species Microcystis aeruginosa and Limnothrix

redekei constituting 82% of phytoplankton bio-

mass persisted for 3 weeks. For the next 3 weeks,

Microcystis aeruginosa and Limnothrix redekei

still co-dominated and with the minor contribution

of Cylindrospermopsis raciborskii made up >80%

of phytoplankton biomass. During the whole per-

iod (August–October), the species composition

was almost unchanged and the total phytoplank-

ton biomass did not change significantly (ANO-

VA, p > 0.05). This phase was different in regard

to the order of dominance (1st Microcystis, 2nd

Lim

noth

rix

rede

kei (

mg

l-1)

0

10

20

30

Temperature (°C)

0 5 10 15 20 25 30

Mic

rocy

stis

aer

ugin

osa

(mg

l-1)

0

5

10

15

Cyl

indr

ospe

rmop

sis

raci

bors

kii (

mg

l-1)

0

5

10

15

Temperature (°C)

0 5 10 15 20 25 30

Aph

anis

omen

on g

raci

le (

mg

l-1)

0

4

8

12

(a) (b)

(c) (d)

Y = 39.93 e-0.101X, r2 = 0.608, p < 0.001 Y = 0.02 e0.217X, r2 = 0.361, p < 0.001

Y = 3.6 x 10-6 e0.505X, r2 = 0.395, p < 0.001

Fig. 3 Phytoplankton dominant species biomass in rela-tion to water temperature in Lake Kastoria duringNovember 1998–October 1999. (a) Limnothrix redekei,

(b) Cylindrospermopsis raciborskii, (c) Aphanizomenongracile, (d) Microcystis aeruginosa

Hydrobiologia (2007) 575:129–140 135

123

Limnothrix or replaced alternatively) in the dif-

ferent water layers and areas of the lake (Fig. 5).

The period is characterized by low light

availability (LI < 0.1) in warm mixed layers (see

Electronic Supplementary Material) and high

concentrations of phosphate phosphorus (0.6 to

1.0 lmol l–1), (Table 1).

Discussion

Phytoplankton flora of Lake Kastoria is poor in

comparison to the rather rich flora of shallow

eutrophic lakes of similar size in the area (Tryfon

& Moustaka-Gouni, 1997; Temponeras et al.,

2000). The low number of species may reflect the

long lasting period of multiple human impacts on

the lake (sewage effluents, hydrological adjust-

ments, fish stock management) resulting in a

strong environmental filter for phytoplankters.

Loss of biodiversity and increase of algal blooms

are the most evident negative ecological impacts

of human activities on the microbial level in

aquatic systems (Paerl et al., 2003). In addition,

the low number of diatoms in the phytoplankton

species list of this shallow lake, in relation with

the rather low silicon concentrations throughout

the year (Table 1), may indicate that past com-

petition has at least partially shaped the phyto-

plankton species pool of the lake (see Sommer,

1990). Of the 33 functional groups described by

Reynolds et al. (2002) and Padisak et al. (2003),

19 were represented in the lake’s phytoplankton.

Diatoms were rare, not only in terms of species

number, but also in terms of biomass (max.

1.2 mg l–1, contributing < 5% to the total phyto-

plankton biomass) (Fig. 2) even during the win-

ter-spring season, the typical period of diatoms

(Sommer et al., 1986). The low diatom biomass is

related to low Si:P < 62.0 and Si:N < 25.0 re-

source ratios during winter (see Electronic Sup-

plementary Material). Nitzschia acicularis

dominated within the diatoms. However, the

biomass of N. acicularis was only 1.4% of the total

phytoplankton biomass, whereas that of Limno-

thrix redekei was 48 times higher. Both species

grow well under low temperatures and low light

availability in mixed layers. However, dominance

of L. redekei has been found associated with

anthropogenic eutrophic conditions in shallow

lakes (Meffert, 1989), while Nitzschia acicularis

perform better in not enriched and deeper mixed

waters (Huszar et al., 2003).

Limnothrix redekei dominance exhibited very

similar patterns in distinct sampling areas and

water layers affecting considerably the patterns of

phytoplankton succession. The similarity of suc-

cession patterns declined when Microcystis aeru-

ginosa, contributing >50% to the total

phytoplankton biomass, formed surface accumu-

lations. Spatial differences (Fig. 5) may arise

through the interaction of the dominants’ behav-

ior (buoyancy regulation, auto-regulated surface

accumulation) and the pelagic zone physical

dynamics under medium speed local winds

(physically induced accumulation).

Limnothrix redekei made up to 99% of the

phytoplankton biomass in winter (Fig. 5) setting

the diversity close to zero (Shannon index based on

biomass Hb = 0.2; Moustaka-Gouni, unpubl.

Axis I (37.7%)-1 0 1 2

Axi

s II

(29

.5%

)

-1.6

-0.8

0.0

0.8

1.6 TEMP N:P

N:LI

NH4-N

NO3-N

PO4-P

Lr + Cr = 10 - 20%Lr + Cr = >20 - 40% Cr = >40%

Lr + Ma = >20 - 40%Lr + Cr + Ag = >40%Lr + Ma = >40%

zmix:zeu

Fig. 4 Two-dimensional PCA ordination of the watersamples of Lake Kastoria during the period of phyto-plankton dominants Limnothrix redekei (Lr), Cylindro-spermopsis raciborskii (Cr), Aphanizomenon gracile (Ag)and Microcystis aeruginosa (Ma), coexistence. Physicaland chemical parameters are indicated as vectors. Abbre-viations: TEMP = water temperature (�C); NO3-N = ni-trate nitrogen (lmol l–1); NH4-N = ammonium nitrogen(lmol l–1); PO4-P = phosphate phosphorus (lmol l–1);N:P = atomic ratio of inorganic nitrogen to phosphorous;N:LI = ratio of inorganic nitrogen to light index; zmix:-zeu = ratio of mixing zone to euphotic zone

136 Hydrobiologia (2007) 575:129–140

123

0

20

40

60

80

100

0

20

40

60

80

% c

ontr

ibut

ion

to t

otal

phy

topl

ankt

on b

iom

ass

0

20

40

60

80

0

20

40

60

80

0

20

40

60

80

Month

N D J F M A M J J A S O0

20

40

60

80

Surface layer Bottom layer

L. redekei M. aeruginosaC. raciborskii A. gracile

0

20

40

60

80

100

0

20

40

60

80

% c

ontr

ibut

ion

to t

otal

phy

topl

ankt

on b

iom

ass

0

20

40

60

80

0

20

40

60

80

0

20

40

60

80

Month

N D J F M A M J J A S O0

20

40

60

80

SSI SSII SSI SSIIS6

S5

S4

S3

S2

S1

S6

S5

S4

S3

S2

S1

1998 1999 1998 1999

Fig. 5 Seasonal succession of phytoplankton species inLake Kastoria during November 1998–October 1999, aspercentage contribution to total phytoplankton biomass.

The shaded areas represent the periods of steady-states(SSI, SSII)

Hydrobiologia (2007) 575:129–140 137

123

data). An extremely low phytoplankton diversity

(zero) has been reported, to the best of our

knowledge, only in one case (Borics et al., 2000).

The main factors that may have promoted and

maintained the persistent steady-state of L. rede-

kei, were relatively stable physical conditions

(mixing at low temperatures) (see Electronic

Supplementary Material) and rather constant (a)

low light conditions (see Electronic Supplemen-

tary Material) and low nutrient concentrations

(Table 1), and (b) low Si:P, Si:N resource ratios

(see Electronic Supplementary Material) for its

possible competitors. Under these conditions, the

specific abilities of species, such as photoadapta-

tion and buoyancy regulation in the water column

(Reynolds et al., 2002), to effectively exploit re-

sources, may have considerably contributed to the

development of this steady-state. Enhanced cell

gas-vacuolation in a large number of L. redekei

trichomes (up to 50% cell volume; Gkelis et al.,

2005), has been observed during the winter.

Moreover, high population densities over the

winter (up to 90 · 106 trichomes l–1), before the

development of daphnids (Moustaka-Gouni et al.,

2006), may be another key factor for establishing

and maintaining overdominance of L. redekei (e.g.

Nicklisch, 1999).

The disruption of the L. redekei steady-state

phase was a consequence of hydraulic flushing of

the lake water (Moustaka-Gouni et al., 2006)

leading to a dramatic drop of total phytoplankton

biomass and a collapse of L. redekei bloom.

Flushing was very effective in breaking the biomass

increase in this sensitive to flushing species (Rey-

nolds et al., 2002). Then, it was not easy for the slow

growing L. redekei population to compensate for

the losses by growth for the next 2 months.

In the summer, intermittent thermal stratifica-

tion maintained a non-steady-state assemblage of

Nostocales and Oscillatoriales, belonging in similar

functional groups (SN and S1). The concentrations

of dissolved inorganic nitrogen declined to very low

values (0.7–3.9 lmol l–1; Table 1). The N:P

resource ratio dropped below the critical ratio of

Redfield, the N:LI ratio reached minimum (8.1; see

Electronic Supplementary Material) and the

nitrogen fixers Cylindrospermopsis raciborskii and

Aphanizomenon gracile dominated (Fig. 5). Their

dominance was shared with the persistent Limno-

thrix redekei whose habitat properties were differ-

ent in the winter–spring period. The decline of L.

redekei under high light availability and dominance

of Cylindrospermopsis raciborskii in nitrogen defi-

cient conditions ( < 0.7 lmol l–1) seems to be the

outcome of their competition. An unusual decrease

of water temperature in late June (Fig. 6) and

heavy rainfall probably disrupted C. raciborskii

biomass increase in the next few weeks. It is well

known that C. raciborskii has a high temperature

optimum for growth (20–30�C) (e.g. Briand et al.,

2004) and can tolerate low light availability in warm

mixed layers (Reynolds et al., 2002). In August,

when high water temperature and poor light

conditions prevailed, a new biomass increase of C.

raciborskii and Aphanizomenon gracile was ob-

served (Figs. 5, 6). In Lake Kastoria, the species A.

gracile behaved like the species Cylindrospermop-

sis raciborskii, which is tolerant to mixing and poor

light conditions. Based on these data, we support

the suggestion of Mischke & Nixdorf (2003) to in-

clude Aphanizomenon gracile into the functional

group SN.

During August–October period, the second

steady-state stage of phytoplankton was observed

with Microcystis aeruginosa and Limnothrix redekei

co-dominants, while Cylindrospermopsis raciborskii

had a minor contribution to the total biomass. Over

J J A S O

Cyl

indr

ospe

rmop

sis

raci

bors

kii (

mg

l-1)

0

2

4

6

8

Cha

nge

in t

he w

ater

tem

pera

ture

(°C

)

-3

-2

-1

0

1

2

3

Month

Fig. 6 Cylindrospermopsis raciborskii biomass in relationto water temperature change observed during the time oftwo consecutive sampling dates, in Lake Kastoria duringJune–October 1999. Values are means and refer to thesurface and bottom layers from all six stations

138 Hydrobiologia (2007) 575:129–140

123

this period a replacement between the two major

species was observed in different water layers and

areas of the lake (Fig. 5). Microcystis aeruginosa

was not detected as a single dominant under the

prevailing poor light conditions (LI < 0.1; Fig. 5

and see Electronic Supplementary Material). Under

these conditions, the dominance and water bloom

formation of this species can be explained by its

tolerance to high insolation at the surface layer and

its ability to regulate buoyancy (Reynolds et al.,

2002). M. aeruginosa differs from Limnothrix rede-

kei in its ability of diel migration that allows Mi-

crocystis aeruginosa to accumulate at the surface

layer. Thus, M. aeruginosa and Limnothrix redekei

partially did not compete, but may have different

niches separated vertically in the water column

(Fig. 5). The main factors of constancy during this

steady-state phase were mixing, low light availabil-

ity and high phosphorus concentrations.

In conclusion, the functional groups S1 (Lim-

nothrix redekei), M (Microcystis aeruginosa) and

SN (Cylindrospermopsis raciborskii, Aphanizom-

enon gracile) which found in steady-state phases in

the highly eutrophic polymictic Lake Kastoria are

in overwhelming dominance worldwide (Naselli-

Flores et al., 2003). However, the dominant spe-

cies Limnothrix redekei in the steady-state phases

in Lake Kastoria has been found, to the best of our

knowledge, as steady-state species only once in

another hypertrophic shallow lake located also in

southern Europe (Rojo & Alvarez-Cobelas,

2003). In Lake Kastoria, two cyanobacteria stea-

dy-states observed within a year and persisted for

almost 4 months under relatively stable physical

conditions. These results are in agreement with a

few studies in tropical (Komarkova & Tavera,

2003) and Mediterranean freshwaters (Naselli-

Flores & Barone, 2003) characterized by long

lasting steady-states of Cyanobacteria and may

indicate relations between climate factors and

phytoplankton dynamics. If the smoother seasonal

changes in irradiance in lower latitudes compared

to those in higher latitudes, in combination with

other properties of warmer climates, are assumed

to result in smoother changes in physical condi-

tions of the lakes, these may allow persistence of

Cyanobacteria steady-states (e.g. Naselli-Florres

et al., 2003). The few results of persistent steady-

states of Cyanobacteria in warmer climates may

have implications for future investigation of cli-

mate impacts on phytoplankton dynamics due to

global warming.

Acknowledgements We thank Judit Padisak and twoanonymous reviewers for constructive comments andhelpful suggestions. This work was partially funded by theMunicipality of Kastoria, Project 7468 of the ResearchCommittee of Aristotle University of Thessaloniki. Wethank all participating members of this project.

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