See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/266321786

Determination of ecological status and ecological preferences of

phytoplankton using multivariate approach in a Mediterranean reservoir

Article in Hydrobiologia · November 2014

DOI: 10.1007/s10750-014-1948-8

CITATIONS READS

9 161

2 authors:

Abuzer Çelekli Baki Öztürk

Gaziantep University Gaziantep University
73 PUBLICATIONS 866 CITATIONS 2 PUBLICATIONS 17 CITATIONS

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Project on Establishment of Reference Monitoring Network in Turkey View project

Investigate of Algae Composition and Limno-Ecological Properties of Alleben Reservoir, TUBITAK Project, ÇAYDAG-112Y002 View project

All content following this page was uploaded by Abuzer Çelekli on 31 October 2014.

The user has requested enhancement of the downloaded file.

Hydrobiologia (2014) 740:115–135
DOI 10.1007/s10750-014-1948-8
PRIMARY RESEARCH PAPER
Determination of ecological status and ecological
preferences of phytoplankton using multivariate approach
in a Mediterranean reservoir
Abuzer Çelekli • Baki Öztürk
Received: 21 September 2013 / Revised: 14 June 2014 / Accepted: 16 June 2014 / Published online: 17 July 2014
Ó Springer International Publishing Switzerland 2014
Abstract The European Union Water Framework
Directive includes phytoplankton as one of the man-
datory five biological indicators to be used to assess
the ecological status of surface waters. The objective
of the study was determination of ecological status and
ecological preferences of phytoplankton from April
2012 to June 2013, using multivariate approach in
Alleben Reservoir in the southeast Turkey. The
reservoir showed a warm monomictic stratification
pattern (stratification in April–October 2012 vs. mix-
ing in November 2012–March 2013). The reservoir
was meso-eutrophic according to phosphorus, chloro-
phyll a, and transparence values. Phytoplankton
biovolume reached remarkable peaks in autumn and
spring. Phytoplankton species belong to functional
groups of A, D, E, J, LO, LM, MP, P, and Y as
descriptor. Phytoplankton trophic index (PTI) and
assemblage index (Q) indicated the overall medium
ecological status of Alleben Reservoir. PTI and
Handling editor: Judit Padisak
Electronic supplementary material The online version of
this article (doi:10.1007/s10750-014-1948-8) contains supple-
mentary material, which is available to authorized users.
A. Çelekli (&)  B. Öztürk
Department of Biology, Faculty of Art and Science,
University of Gaziantep, 27310 Gaziantep, Turkey
e-mail: celekli.a@gmail.com
B. Öztürk
e-mail: bakiozturk27@hotmail.com
Q indices may be appropriate phytoplankton metrics
to assess the ecological status of the reservoir.
Changes in environmental gradients significantly
influenced the ecological preferences of species and
phytoplankton abundance in the reservoir. Canonical
correspondence analysis (CCA) confirmed that phy-
toplankton species were sensitive to environmental
variability, with the first two axes of CCA able to
explain 92.8% of the total variation and 37.1% of the
cumulative percentage variance in the phytoplankton
assemblage structure. Most effective explanatory
factors (e.g., salinity, conductivity, pH, and tempera-
ture) played significant role (P = 0.002) in the
seasonality of species.
Keywords Mediterranean Reservoir  Ecological
status  Ecological preferences  Functional group 
Phytoplankton
Introduction
The seasonality of phytoplankton is characterized by
sequences of dominant organisms. The triggers for the
change from one dominant to another have fascinated
plankton ecologists for more than 70 years (Reynolds,
2006). These have been progressively rationalized,
with two major kinds of change: those that are
allogenically driven by abrupt stochastic external
events, such as storms or floods, and those that reflect
123
116
gradual changes in the environment, generally those
brought about as a consequence of the interacting
activities of the organisms. The latter are thus
supposed to be autogenic and they comply with
patterns understood to be those of succession (Rey-
nolds, 1980). Seasonal succession in the freshwater
phytoplankton typically embodies a shift in domi-
nance from small r-selected forms at their initiation to
large K-selected organisms, often dominating toward
the end of stable phases of thermal stratification
(Reynolds, 1984). Unstable environmental conditions,
with full water circulation, relatively low light inten-
sity, and high of nutrients availability are also
exploited by tolerant r-selected species.
These seasonal changes in phytoplankton compo-
sition are strongly influenced by intra-annual patterns
and variations in the weather and in the associated
physicochemical consequences (Hutchinson, 1967;
Dokulil & Teubner, 2003; Reynolds, 2006; Zohary
et al., 2010). However, even if the selection processes
are broadly understood, prediction of dominance at the
species level is generally difficult, save on the basis of
precedent. For much of the time, the phytoplankton
constitutes a great diversity of species, present in
variable abundance (Wetzel & Likens, 2000; Abran-
thes et al., 2006). Each may respond to temporal and
spatial variability in environmental factors, both biotic
and abiotic (Horne & Goldman, 1994; Honti et al.,
2007; Zohary et al., 2010), even though knowledge of
the ecological requirements of the organisms based on
long-term data is generally rather poor (Dokulil &
Teubner, 2003; Alvarez Cobelas et al., 2005; Babana-
zarova & Lyashenko, 2007; Naselli-Flores and Ba-
rone, 2007; Padisák et al., 2010). This is, in any case, a
severe omission but it also misses the opportunity to
use algal abundance and dynamics as a useful
biological tool for evaluating water quality (Rakoc-
evic-Nedovic & Hollert, 2005; Reynolds, 2006).
Information about the composition, abundance, and
biovolume of phytoplankton is being applied to the
assessment of trophic condition in water bodies. Many
studies of temporal and spatial distribution indicate that
the ecologies of specific algae are influenced by specific
environmental preferences (Reynolds, 1984; Hall &
Smol, 1992). However, this information is still far from
complete, and there remains a need for long-term data
that may better define species-specific ecological pref-
erences. Understanding has been assisted through
observations on the simultaneous dynamic reactions of
123
Hydrobiologia (2014) 740:115–135
group of species to the same environmental variations,
and these have provided a surprisingly sensitive means
of classifying both ecologically similar species and the
environmental conditions under which they flourish;
moreover, dynamics of these functional groups respond
in similar ways to various sets of environmental
stressors (Reynolds et al., 2002; Padisák et al., 2006).
In this way, studies of phytoplankton and their season-
ality are becoming a significant tool in limno-ecological
monitoring (Reynolds et al., 2002; Padisák et al., 2003;
Istvánovic et al., 2005; Padisák et al., 2006, 2009). It is
sometimes difficult to differentiate the compounded
effects of several environmental factors operating
simultaneously, but the use of multivariate approaches
allows some prediction to be made about the cumulative
impacts of multiple stressors on primary production and
trophic behavior (Kruk et al., 2002; Abranthes et al.,
2006 Çelekli, 2006). Several long-term monitoring
studies have invoked such methods to relate the
seasonality of the phytoplankton to contemporaneous
variations in the environment, and these have also
helped to define better the habitat requirements of the
algae (e.g., Forsström et al., 2005; Salmaso and Padisák,
2007; Padisák et al., 2010). These approaches also
reinforce ecological classification of the phytoplankton
species, the functional groupings of which interrelated
the ecologies, morphologies, and physiologies common
to the members constituting each group, and which,
arguably, underpin their seasonality and their dynamics
in particular water bodies (Reynolds et al., 2002).
The European Water Framework Directive (WFD)
outlines the ecological status of surface waters to be
assessed through the analysis of various characteristics
of aquatic flora and fauna (Directive, 2000; EC, 2009).
Annex V of the WFD specifically requires that
ecological status of phytoplankton in lentic ecosys-
tems should be assessed using biovolume, composi-
tion, and chlorophyll a (EC, 2009; Poikane et al.,
2011; Phillips et al., 2013). In many countries of
Europe, the national assessment systems for phyto-
plankton in lakes and reservoirs, however, still lack
metrics for phytoplankton composition (Poikane,
2009, Birk et al., 2012).
Several limno-ecological studies regarding phyto-
plankton have been carried out in Mediterranean
region (Naselli-Flores, 2003; Moreno-Ostos et al.,
2008; Hoyer et al., 2009; Becker et al., 2010; Katsiapi
et al., 2011; Molina-Navarro et al., 2014). Very rich
limnosystems are present in Mediterranean region,
Hydrobiologia (2014) 740:115–135
although knowledge about ecology of the organisms
with long-term monitoring is generally rather poor
(Alvarez Cobelas et al., 2005). From that point, the
present study regarding phytoplankton or limno-
ecology in Alleben Reservoir is the first study of this
kind in the southeast of Turkey. The present study, part
of a programme of limnological investigations cen-
tered on the southeast region of Turkey, sets out to
explain some distinctive features of the phytoplankton
of Alleben Reservoir. Here, main objectives of the
study were as follows: (i) to determine phytoplankton
composition; (ii) to use phytoplankton metric to
establish the ecological status of Alleben Reservoir,
(iii) to analyze the relationship between biovolume of
phytoplankton species and limno-ecological charac-
teristics; and (iv) to estimate ecological preferences of
species for measured variables with using multivari-
able techniques, based on regular monitoring carried
out in the reservoir for 15 months.
Materials and methods
Alleben Reservoir (Fig. 1) is located at 939 m.a.s.l.,
14 km the southwest Gaziantep City, and in the
southeast Turkey (37°40 2900 N and 37°160 2000 E). The
reservoir was built on a wetland area in 1995s where
water was aimed to be stored for the irrigation of
agricultural uses, prevention of flooding, and recrea-
tional territory (Fig. 1).
Fig. 1 Map of Alleben Reservoir and location of the sampling stations
117
Sport complex and restaurant are present near to the
reservoir, whereas villas are located far away from the
reservoir. Sport complex has a water treatment
facility, whereas restaurant and villas have not. The
characteristics of reservoir are maximum depth (Zmax):
15.6 m, mean depth (Zmean): 7.5 m, surface area:
0.34 km2, volume: 2.55 hm3, and catchment area:
0.62 km2. Retention time was calculated theoretical as
0.76 years and obtained from the General Directorate
of State Hydraulic Works (DSI, Turkey). The region is
characterized by a semiarid Mediterranean climate,
and water influx (Sacır creek) to the reservoir is
confined to the winter and spring months due to rainy
winter and spring followed by very dry summers.
Between April 2012 and June 2013, water samples
were taken at monthly intervals at each of five stations
(Fig. 1), from just beneath of the surface for biological
and physicochemical analyses. Vertical water samples
were taken from the 5th station (each meter of a depth
profile), using a 2.5-l Hydrobios water sampler bottle
to determine the changes in temperature and DO
profile of water column during the study time and so to
predict the water mixing regime of this reservoir.
Environmental variables were measured in situ: tem-
perature, oxygen concentration, saturation, conduc-
tivity, salinity, pH, redox potential, and total dissolved
solid (TDS), using an YSI–556 oxygen-temperature
meter from just beneath the surface in five stations and
the each meter of a depth profile in 5th station. Water
transparency was monthly measured using a 20-cm
123
118
Secchi disk during the study period. Geographical data
(elevation, latitude, and longitude) were read from a
geographical positioning system. Atmospheric tem-
perature and precipitation values were obtained from
Gaziantep Meteorological Station, which is 10 km
away from the southeast Alleben Reservoir.
Samples were stored in coolers with ice packs,
pending transfer to the laboratory, where they were
analyzed for chlorophyll content and selected chem-
ical determinants. Chlorophyll a concentrations were
determined by spectrophotometer after extraction in
90% methanol (Youngman, 1978). Analyses of chem-
ical variables (N–NH4, N–NO3 N–NO2, P–PO4, and
SO4) and microbiological test (total coliform bacteria)
were carried out by standard methods (APHA
AWWA, 1989). After Sartorius filtration technique,
chemical analyses of water samples were done by use
of ion chromatography (Thermo Scientific Dionex
ICS-5000, HPIC system). Heavy metals were ana-
lyzed using inductively coupled plasma-optical emis-
sion spectrometry (ICP-OES, Perkin-Elmer, Optima
2100 DV). Water samples were incubated for 5 days at
20°C in a dark place, in order to determine biological
oxygen demand (BOD5) (APHA, 1989). Turbidity of
water was measured nephelometrically and expressed
in NTU. The taxonomic keys (Ettl, 1983; Komárek &
Fott, 1983; Popovsky & Pfiester, 1990; Krammer &
Lange-Bertalot, 1991a, b; Komárek & Anagnostidis,
1998; Krammer & Lange-Bertalot, 1999a, b; John
et al., 2002; Wehr & Sheath, 2003) were consulted to
assist phytoplankton identification. Identification of
phytoplankton taxa was carried out by the use of
Olympus light microscope (Olympus BX53) attached
DP73 model digital camera with imaging software
(Olympus CellSens Vers. 1.6). The sub-samples for
phytoplankton enumeration were preserved in poly-
ethylene bottles with acetic lugol-glycerol solution.
Sub-samples (20–100 ml) were allowed to settle for
24–48 h in counting chamber and then enumerated
(two transects) at magnifications of 400–6009 (3
replicates) under an inverted microscope (Olympus
CKX41) (Utermöhl, 1958). At least 350 settling units
of the most abundant species were enumerated in
every sample. Phytoplankton biovolume was esti-
mated from abundance data and measurements of
specific cell volume taken approximating geometric
shapes of cells (Rott, 1981; Hillebrand et al., 1999;
Sun & Liu, 2003). Dimensions of the least 25
individuals were measured, and the mean volume of
123
Hydrobiologia (2014) 740:115–135
each taxon was multiplied by the corresponding
concentration to derive species-specific standing-crop
volumes. Phytoplankton species were assigning into
functional groups following the criteria of Reynolds
et al. (2002) and Padisák et al. (2003, 2006, 2009).
Species with high frequency and comprising more
than 10% of the total biovolume were considered to
represent the significant presence of its ascribed
dominant group.
Organization for Economic Cooperation and
Development (OECD) criteria (Vollenweider & Kere-
kes, 1982) and Carlson (1977) trophic state index
methods were utilized in order to calculate the trophic
state of reservoir based on values of chlorophyll a and
Secchi disk depth. Besides, phytoplankton biovolume
was used to assess the trophic state of reservoir.
Phytoplankton trophic index (PTI) and phytoplank-
ton assemblage index (Q) were used to assess the
status of Alleben Reservoir according to the Water
Framework Directive. PTI value was calculated by the
use of following equation (Eq. 1) from the proportion
taxa corresponding to total biovolume (Philips et al.,
2013).
Pn
j¼1 aj sj
PTI ¼ Pn ; ð1Þ
j¼1 aj
where aj is proportion of jth taxon in the sample and sj
is the optimum of jth taxon in the sample.
The assemblage index (Q index) values were
determined by following an equation (Eq. 2) proposed
by Padisák et al. (2006) from the proportion taxa
corresponding to total biovolume.
X
n
Q¼ pi F; ð2Þ
j¼1
where pi is the relative share (where pi = ni/N; ni is
biovolumes of the ith functional group; N is the total
biovolume) of functional groups in total biovolume.
F (ranging from 0 to 5) is a factor number
established for the ith functional group in the given
lake type (Padisák et al., 2006). All the functional
groups were used to obtain Q index. In order to
Q index based on the factor F weights assigned to
each functional group, lake type 1 (calcareous,
average depth 3–15 m, and persistent) in Padisák
et al. (2006) was selected because the characteristics
of this type are similar to the Alleben Reservoir.
However, the Alleben limno-Reservoir has a lower
Hydrobiologia (2014) 740:115–135
surface area. Five levels of classification for the
Q index were used as 0–1, poor ecological status;
1–2, tolerable; 2–3, medium; 3–4, good; and 4–5:
excellent.
Pearson’s correlation was used to test the relation-
ships among the environmental variables. Besides, this
test was also used to evaluate the correlations among
PTI, Q index, biovolume, chlorophyll a, phosphate,
Secchi depth, and Carlson’s trophic state. Canonical
correspondence analysis (CCA), a direct gradient ana-
lysis technique, was used to elucidate the relationship
between predictor variables (environmental factors)
and the response variables (phytoplankton species) in
the reservoir. Following ter Braak & Smilauer (1998),
unimodal response models were employed for the
ordination of analyses along long gradients. Environ-
mental variables were transformed (ln (x ? 1), except
for pH) to reduce skewness (ter Braak & Smilauer,
1998). For statistical analysis of data, all taxa over 1%
of total phytoplankton biovolume, which corresponded
to the abundant species, were considered (ter Braak,
1995). The significance of environmental variables to
explain the variance of species data in CCA was tested
using forward selection of Monte Carlo simulations
with 499 unrestricted permutations. Significant vari-
ables at P \ 0.01 were performed for CCA analysis.
Thus, CCA analysis included 17 species of phyto-
plankton, 8 environmental variables, and 15 sampling
time (months) as supplementary variables. Seventy-
five of sampling data (5 stations 9 15 months) were
carried out for CCA analysis. The program CANOCO
was used for the ordination analyses (ter Braak &
Smilauer, 1998; Leps & Smilauer, 2003). Weighted
averaging regression of CALIBRATE program (Jug-
gins & ter Braak, 1992) was used to estimate species
optima (uk) and tolerance (tk) levels for environmental
variables. Objective of calibration is to estimate values
of environmental descriptors on the basis of species
composition. For this purpose, weighted averaging
method is commonly used for the estimates of species
optima in relation to selected environmental gradient.
Weighted-average metrics assess only a single pres-
sure (e.g., nutrients) or related pressures of environ-
mental factors on organisms. Besides, calibration is
also one of the steps used in more complicated
analyses, such as ordination methods (Leps & Smil-
auer, 2003). Some phytoplankton species comprising
only its one occurrence (rare species) and having
119
negligible biovolume value (\1% of total biovolume)
throughout the study were not taken in analyses.
Results
Physicochemical and limnological variables
Physicochemical variables are given in Table 1. The
water in Alleben Reservoir was slightly basic; pH
readings ranged between 6.68 and 8.72 (mean
7.88 ± 0.51). Phosphate (PO4–P) varied seasonally
with high values during complete water circulation,
but it was observed to fall to concentrations
(13.78 lg l-1) in October 2012. Among nitrogen
species, ammonium (NH4–N) reached high values in
the autumn–winter period, while nitrate (NO3–N) fell
from 0.83 mg l-1 in the winter to 0.32 mg l-1 in the
summer. Minimum and maximum conductivities (EC)
of 278.0 and 414.0 lS cm-1 were noted in September
2012 and May 2013, respectively.
Water thermal structure (Fig. 2a) by the depth
distribution of isotherms relative to the surface season-
ally changed during the study period. The reservoir was
thermally stratified between April and October in 2012.
The full circulation period usually begins in November
2012 and ends in March 2013. The distribution of
dissolved oxygen concentration is tabulated in Table 1;
readings ranged from 0.98 to 13.85 mg l-1, decreasing
especially in the summer hypolimnion (Fig. 2b). Mean
ratio of mixing depth to euphotic depth (Zmix/Zeu) had
1.31 ± 0.79 m and increased in the autumn–winter
period. Significant variation in this ratio among seasons
was found (P \ 0.05).
Trophic state and ecological status
Value of chlorophyll a was generally higher in the
spring and late autumn, but fell to low values in the
summer and early autumn. This variable changed
monthly from 4.98 to 23.50 lg l-1 for October 2012
and November 2012, respectively. Total phytoplank-
ton biovolume (9106 lm3 l-1) varied between 64.3
and 290.1 for October 2012 and November 2012,
respectively. Water transparence changed between
1.10 m and 3.32 m (mean 1.93 ± 0.49 m). The res-
ervoir was meso-eutrophic according to phosphorus,
chlorophyll a, and transparence values, whereas it was
123
120 Hydrobiologia (2014) 740:115–135

Table 1 Minimum, Unit Minimum Maximum Mean ± SD

maximum, and mean ± SD
(standard deviation) values Temperature °C 6.65 26.92 14.72 ± 5.27
of environmental and
Conductivity lS cm-1 278.0 414.0 333.2 ± 38.4
biological variables
combined from sampling TDS g l-1 0.18 0.27 0.22 ± 0.03
stations in Alleben Salinity ppt 0.13 0.20 0.16 ± 0.02
Reservoir Turbidity NTU 0.76 6.78 3.05 ± 1.18
DO mg l-1 0.98 13.85 8.26 ± 3.18
pH 6.68 8.72 7.88 ± 0.51
ORP mV -169.93 163.30 -52.44 ± 79.18
BOD5 mg l-1 1.18 7.00 4.21 ± 1.82
Chlorophyll a lg l-1 4.98 23.50 11.49 ± 4.32
-1
PO4 lg l 13.78 23.38 17.04 ± 2.52
NO3 mg l-1 0.24 0.88 0.49 ± 0.16
NO2 mg l-1 0.05 0.16 0.08 ± 0.01
NH4 mg l-1 0.01 0.90 0.12 ± 0.16
Mg mg l-1 4.63 11.56 8.52 ± 1.68
Ca mg l-1 21.57 74.68 48.78 ± 13.82
Na mg l-1 0.01 4.79 3.39 ± 0.95
Cl mg l-1 2.14 5.36 4.17 ± 0.90
SO4 mg l-1 5.18 15.50 10.63 ± 2.23
Al lg l-1 0.00 83.00 16.88 ± 22.68
Fe lg l-1 0.00 167.00 39.79 ± 29.61
-1
Ni lg l 0.00 13.00 1.96 ± 3.14
Mn lg l-1 0.00 133.00 16.17 ± 29.44
Cyanide mg l-1 0.00 0.02 0.003 ± 0.010
Secchi depth m 1.10 3.20 1.93 ± 0.49
Total biovolume 106 lm3 l-1 64.3 290.1 184.1 ± 15.2
Hardness mmol l-1 0.74 1.98 1.58 ± 0.24
Precipitation mm 0.00 259.40 43.87 ± 67.32
Air temperature °C 4.90 31.60 19.47 ± 9.00
Zmix/Zeu m 0.58 2.67 1.31 ± 0.79

oligotrophic state according to value of total phyto-
plankton biovolume (Table 2). Value of PTI varied
from 0.25 to 1.47 for October 2012 and November
2012, respectively. PTI was positively correlated with
phytoplankton biovolume (P \ 0.01, r = 0.758), PO4
(P \ 0.01, r = 0.881), and chlorophyll a (P \ 0.01,
r = 0.793). The F weights for each functional group
identified appear in Table 3. The assemblage index (Q
index) ranged from 2.60 to 3.42 (mean 2.91) during the
study period. This indicated a medium ecological
status of Alleben Reservoir during the study period.
Q index was positively correlated with chlorophyll
a (P \ 0.01, r = 0.731), PO4 (P \ 0.01, r = 0.860),
phytoplankton biovolume (P \ 0.05, r = 0.542), and
Zmix/Zeu ratio (P \ 0.05, r = 0.590). Plots of indices
vs. phytoplankton biovolume, phosphate, and chloro-
phyll a are given in Fig. 3a–f. Results indicated that
both indices had the strong regression with aforemen-
tioned trophic state indicators for the total set of
samples.
Seasonality of phytoplankton
With regard to the counts of phytoplankton, a total of
76 species in Alleben Reservoir belonging to 20
functional groups were recorded during study period
(Appendix 1—Supplementary Material). Nine func-
tional groups: A, D, E, J, LO, LM, MP, P, and Y were

123
Hydrobiologia (2014) 740:115–135 121

Fig. 2 Isopleths of (a) temperature and (b) dissolved oxygen with superimposed variation of vertical station at Alleben Reservoir
during the study period. Abbreviations indicate the code of each month (e.g., April 2012 (Ap12) and May 2013 (M13), etc.)

Table 2 Trophic state of Alleben Reservoir

Authors Variables Trophic state

Vollenweider & Kerekes (1982) Chlorophyll a Eutrophic

Secchi depth Eutrophic
Carlson (1977) TSIChlo Eutrophic
TSISD Meso-eutrophic
Brettum (1989) Phytopl. biovol. annual maximum Oligotrophic
Heinonen (1980) Phytopl. biovol. annual average Oligotrophic
Rott (1984) Phytopl. biovol. annual maximum Oligotrophic
TSIChlo and TSISD are trophic state indices of chlorophyll a and Secchi depth, respectively

Table 3 Descriptor phytoplankton species with their taxonomic and functional groups according to Reynolds et al. (2002) and
Padisák et al. (2003, 2006, 2009), and the factor F weights for each functional group for the Alleben Reservoir (2012–2013)
Functional group Descriptor species Taxonomic group F

B Cyclotella iris, C. planctonica Heterokontophyta 3

D Fragilaria biceps Heterokontophyta 2
E Dinobryon divergens Heterokontophyta 2
J Tetraedron sp. Chlorophyta 1
LO Peridinium cinctum Myzozoa (Dinoflagellata) 1
LM Ceratium hirundinella Myzozoa (Dinoflagellata) 0
MP Fragilaria ulna Heterokontophyta 5
P Fragilaria crotonensis Heterokontophyta 5
Y Cryptomonas ovata Cryptophyta 2

123
122
Fig. 3 PTI vs. (a) total phytoplankton biovolume, (b) chloro-
phyll a, and (c) PO4. Q index vs. (d) total phytoplankton
biovolume, (e) chlorophyll a, and (f) PO4
found as descriptor and were consequently evaluated
in phytoplankton composition of Alleben (Table 3).
Temporal variations in the algal biovolume are plotted
in Fig. 4a. Phytoplankton biovolume showed temporal
variation and had remarkable peaks in autumn and
123
Hydrobiologia (2014) 740:115–135
Fig. 3 continued
spring (Fig. 4a). Total phytoplankton biovolume
(9106 lm3 l-1) ranged between 64.3 and 290.1 (mean
184.1 ± 15.2). The lowest total biovolume was found
in October 2012, while the highest value was deter-
mined in November 2012 (began water mixing
period).
Hydrobiologia (2014) 740:115–135 123

Fig. 4 Temporal variations

in (a) the biovolume of algal
classes and (b) relative
contribution of dominant
algal species to total
biovolume. The codes of
each month are given in
Fig. 2. Abbreviations of
phytoplankton species are
cyli, Cyclotella iris; cylp, C.
planctonica; frab, Fragilaria
biceps; tet, Tetraedron sp.;
perc, Peridinium cinctum;
din, Dinobryon divergens;
and others, others species

Relative contributions of phytoplankton species to
total biovolume are given in Fig. 4b. The diatom
species in the reservoir were usually found during the
entire study period. Phytoplankton species; the dia-
tom, especially Cyclotella planctonica, C. iris, and
Fragilaria biceps (for taxonomic authorities, see
Appendix 1—Supplementary Material); the dinofla-
gellate, Peridinium cinctum; the chlorophyts Tetrae-
dron sp.; and the chrysophytes, Dinobryon divergens
had important contribution to the total biovolume.
Both mentioned Cyclotella species were major frac-
tions of biovolume value during thermal stratification
and complete water circulation in Alleben Reservoir.
F. biceps strongly developed in April 2012 and 2013,
while the chlorophyts whose main representative is
Tetraedron sp. has high biovolume peaks in May
2012, September 2012, and May 2013. The dinofla-
gellate P. cinctum had remarkable peaks in June 2012,
September 2012, and June 2013, while the chryso-
phytes, dominated by D. divergens, developed in
November 2012. During study period, other species
given in Fig 4b such as Fragilaria crotonensis,
Fragilaria construens, Fragilaria ulna, Scenedesmus
communis, Pediastrum boryanum, Pediastrum duplex,
Mougeotia parvula, Chlamydomonas lapponica, Pla-
gioselmis nannoplanctica, Peridiniopsis cunningtonii,

123
124 Hydrobiologia (2014) 740:115–135

Oscillatoria limosa, Oscillatoria formosa, and Gymn-

odinium uberrimum had low contribution to total
phytoplankton biovolume of Alleben Reservoir. Cya-
nophyceae species had mainly high biovolume in the
summer period.

Correspondence analysis of phytoplankton

and environment

Multivariate statistical approaches were used to eval-

uate the relationship between biovolume of phyto-
plankton assemblages and environmental variables in
the reservoir. A total of 37.1% of cumulative variance
in species data was explained by the first two CCA
axes, with over 92.8% of the correlations between
predictor variables (environmental factors) on the
response variable (phytoplankton species). Applica-
tion of forward selection using the Monte Carlo test
confirmed that first two axes were highly significant
(P = 0.002, F = 11.827) (Table 4). Most effective
explanatory factors (as in descending order, salinity,
conductivity, pH, temperature, TDS, Ca, and PO4)
played significant role (P = 0.002) on the seasonality
of species.
With regard to the ordination (Fig. 5), salinity,
temperature, pH, conductivity, and phosphate were the
most important variables governing the seasonal
succession of phytoplankton. The distribution of main
algal occurrences in the same ordination showed also
the proximity of large pennate diatoms, F. biceps, F.
crotonensis, F. ulna, and Navicula cryptocephala to
the main axis, at the higher PO4 values in April 2012,
May 2012, and May 2013. On the other hand,
Cyclotella species were located closer to Ca arrow
Fig. 5 Ordination diagram of canonical correspondence ana-
lysis (CCA) showing biovolume of phytoplankton taxa and
selected environmental variables (arrows) during sampling
months (up triangular). Abbreviations are given in Fig. 2 and
Appendix 1—Supplementary Material. Symbols of the chloro-
phyts, the diatoms, the dinoflagellates, the chrysophytes, and the
cryptophytes are square, circle, down triangle, X mark, and star,
respectively
(Fig. 5). With regard to dinoflagellate, Ceratium
hirundinella was associated mainly with higher tem-
perature, forming near to the summer months in the
ordination. Furthermore, based on the weighted aver-
ages of ordination values, estimated solutions of the
species-specific optima (uk) of each determinant and
the levels tolerated (tk), as entered in Table 5, show
that C. planctonica, C. iris, Tetraedron sp., F. biceps,
D. divergens, and P. cinctum with high N2 were the

Table 4 Main results of canonical correspondence analysis (CCA) using Monte Carlo permutation test for biovolume phytoplankton
species–environment variables relationship
Axes k1 k2 k3 k4 Total inertia

Eigenvalues 0.354 0.278 0.162 0.100 1.699

Species–environment correlations 0.967 0.928 0.845 0.889
Cumulative percentage variance
Of species data 20.8 37.1 46.7 52.6
Of species–environment relation 32.2 57.5 72.3 81.4
Sum of all eigenvalues 1.699
Sum of all canonical eigenvalues 1.097
Test of significance of first canonical axis: eigenvalue = 0.354
F = 11.827 P = 0.002

123
 Table 5 Optimum and tolerance values of phytoplankton taxa were determined by using weighted average regression in Alleben Reservoir. uk and tk indicated optima and
tolerance, respectively
Code C Max. N2 Temp (°C) Cond (lS TDS Salinity DO pH PO4 NO3 SO4 Ca (mg l-1)
cm-1) (g l-1) (ppt) (mg l-1) (lg l-1) (mg l-1) (mg l-1)
uk tk uk tk uk tk uk tk uk tk uk tk uk uk uk tk uk tk uk tk
Hydrobiologia (2014) 740:115–135

cyli 60 124927 42.48 15.97 6.59 346.50 43.77 0.22 0.03 0.16 0.02 10.50 1.47 7.93 0.48 16.79 2.28 0.47 0.17 11.33 2.46 53.92 14.21
cylp 56 213192 23.53 13.16 6.71 356.88 48.17 0.23 0.03 0.17 0.02 11.30 1.67 8.04 0.41 16.38 1.81 0.52 0.21 12.02 2.49 57.06 13.11
frab 55 68861 31.36 15.51 4.99 345.35 31.73 0.23 0.02 0.17 0.02 10.60 1.30 7.76 0.55 18.45 2.65 0.51 0.17 10.62 2.72 48.38 15.43
frac 22 7841 14.18 19.52 3.02 339.24 16.81 0.23 0.02 0.17 0.02 9.65 0.58 7.30 0.36 18.65 2.75 0.55 0.16 9.57 2.42 35.41 13.72
frau 24 66131 11.00 17.95 2.87 343.94 16.66 0.24 0.02 0.18 0.02 9.90 0.51 7.11 0.38 19.73 2.28 0.44 0.19 7.90 2.91 40.10 13.67
navc 25 12224 5.36 16.55 3.27 343.57 24.33 0.24 0.02 0.18 0.02 10.19 0.74 7.07 0.62 19.88 2.30 0.33 0.14 6.53 2.61 48.62 9.52
chlp 7 10299 5.22 22.90 2.69 314.00 22.55 0.21 0.02 0.14 0.01 9.20 0.63 8.10 0.36 15.94 2.39 0.54 0.13 10.14 1.30 48.07 5.58
pedb 21 11164 8.45 21.10 2.86 293.47 29.96 0.19 0.02 0.14 0.02 9.70 0.52 8.30 0.30 15.50 1.94 0.40 0.11 9.75 1.14 42.82 7.73
pedd 6 16406 3.27 22.69 2.93 290.80 6.97 0.19 0.00 0.14 0.01 9.43 0.47 8.45 0.22 14.41 0.53 0.45 0.03 9.15 0.42 43.22 1.29
tet 60 71712 32.92 18.87 3.93 326.82 28.80 0.22 0.03 0.16 0.02 9.82 0.72 7.68 0.56 17.96 2.94 0.50 0.15 9.95 1.98 39.19 13.43
cer 15 28570 6.69 24.91 3.67 297.45 24.04 0.20 0.02 0.14 0.01 8.63 0.65 7.50 0.42 15.74 2.13 0.47 0.14 9.42 1.44 42.16 7.40
gym 4 35168 3.00 21.89 0.17 279.76 2.84 0.18 0.00 0.13 0.02 9.52 0.17 8.38 0.06 14.96 0.16 0.34 0.03 9.39 0.05 42.84 0.57
percu 18 36925 8.39 23.16 2.15 308.90 23.50 0.20 0.02 0.14 0.01 9.05 0.50 7.87 0.42 16.01 2.33 0.58 0.19 10.00 0.96 46.05 8.28
perc 43 191179 22.61 19.31 6.09 317.30 30.34 0.21 0.02 0.15 0.01 9.80 1.31 8.01 0.37 16.31 2.01 0.52 0.14 10.43 1.41 49.31 8.18
din 55 177331 13.57 18.38 4.78 312.04 22.44 0.20 0.02 0.14 0.01 9.75 0.80 7.90 0.46 15.90 1.77 0.49 0.12 10.06 1.29 45.93 6.39
cry 60 22558 26.33 14.56 5.89 342.00 36.78 0.22 0.02 0.16 0.02 10.82 1.56 7.80 0.47 17.64 2.38 0.55 0.19 10.88 2.45 49.32 14.20
mou 1 69144 1.00 21.86 3.91 284.00 25.61 0.18 0.02 0.13 0.02 9.47 0.85 8.46 0.40 15.15 2.04 0.37 0.14 9.36 1.75 43.70 9.54
RMSE 3.68 24.54 0.02 0.01 0.81 0.33 1.77 0.12 1.53 7.98
R2 0.62 0.58 0.58 0.66 0.62 0.58 0.50 0.41 0.52 0.66
C showed counting number of species, N2 is Hill’s diversity, and codes of species are given in Appendix 1—Supplementary Material
125

123
126
most frequently occurring species in Alleben Reser-
voir. Cyclotella species and C. ovata were mainly
found in cooler water, while Peridinium species and
C. hirundinella preferred warmer water during study
period. Species of Fragilaria preferred higher PO4
value than those of other phytoplankton taxa. Further-
more, Cyclotella species were found in harder water,
comparing other phytoplankton taxa.
Discussion
Physicochemical and limnological characteristics
Temporal changes in the water column movements in
lentic systems are one of the main environmental
forces (Reynolds, 1984; Barbosa & Padisák, 2002;
Reynolds, 2006). It is known that heat in aquatic
ecosystems had two physical functions as establish of
thermal stratification and water mixing. Absorption of
solar energy by the water bodies seasonally changed,
which caused to the water circulation. Four seasons are
observed in Mediterranean region, so air temperature
is mainly high and photoperiod is long in period of the
between late spring and earlier autumn. This Medi-
terranean climate can undergo the long stratification
period in water bodies. Water circulation, stratification
in April–October 2012 vs. mixing in November 2012–
March 2013, indicated that Alleben Reservoir was
warm monomictic characteristic. Same water circula-
tion (stratification vs. mixing) pattern was also found
for several reservoirs in the Mediterranean region such
as Sau Reservoir (Becker et al., 2010), El Gergal
Reservoir (Moreno-Ostos et al., 2008; Hoyer et al.,
2009), and Pareja limno-Reservoir (Molina-Navarro
et al., 2014). Reynolds (2006) reported that phyto-
plankton growth is mainly related to availabilities of
light and nutrients, which driven by the mixing
regime. The mixing regime in the present study not
only affected physicochemical variables (e.g., light
and nutrients), but also affected phytoplankton
dynamics (e.g., their seasonality based on the avail-
ability of growth-limiting resources and buoyance).
The mixing period in the winter and the premixing in
the late autumn in Alleben limno-Reservoir could
affect light availability which could play a limiting
factor for phytoplankton growth. The long stratifica-
tion period in this reservoir could led to high light
availability in the epilimnion, whereas P-limitation for
123
Hydrobiologia (2014) 740:115–135
phytoplankton growth could be determined in this
period due to consuming available phosphate by
phytoplankton. Effect of mixing regime on availability
of the light and nutrients was observed in Mediterra-
nean water bodies as Sau Reservoir (Becker et al.,
2010) and Pareja limno-Reservoir (Molina-Navarro
et al., 2014). Alleben Reservoir had a low transparency
(mean 1.93 ± 0.49 m). Chlorophyll a, phosphate, and
conductivity values were generally higher during
water mixing period, but fell to low values in the
summer and early autumn. The overturning and
upwelling of the hypolimnetic nutrients through the
mixing regime in the reservoir could increase phyto-
plankton biovolume and chlorophyll-a and decrease
Secchi depth.
Trophic state and ecological status
Alleben Reservoir showed characteristic of meso-
eutrophic (Table 2) with respect to the chlorophyll
a and Secchi depth that it supported by criteria of
OECD (Vollenweider & Kerekes, 1982) and the
solution of Carlson’s Trophic State Index (TSI)
(Carlson, 1977). Phytoplankton organisms give sensi-
tive responses to the changes of water quality
(Hutchinson, 1967; Reynolds, 1984; Willen, 2000;
EC, 2000). For this reason, Willen (2000) presented
that phytoplankton biovolume as indicators for assess-
ing the links between phytoplankton and the environ-
ment can be used to evaluate water quality. With
regard to phytoplankton biovolume, Alleben Reser-
voir conformed to the maxima typical (Brettum,
1989), levels in mid-summer (Heinonen, 1980) and
the basis of the annual average of phytoplankton
biovolume (Rott, 1984) were also similar to those said
to typify oligotrophic systems (Table 2). Total phyto-
plankton biovolume could be limited due to the hard
water of reservoir. Cyanobacterial biovolume (\1%)
had no significant contribution to total phytoplankton
biovolume in Alleben Reservoir. EC (2009) reported
that species of cyanobacteria associated with eutro-
phic conditions were considered for the percent
contribution of cyanobacteria as a metric. Phytoplank-
ton biovolume and Secchi depth values in Alleben
Reservoir was similar to an oligo-mesotrophic Med-
iterranean Pareja limno-Reservoir (Molina-Navarro
et al., 2012, 2014); however, Alleben Reservoir had
higher chlorophyll a value. Whereas, Alleben Reser-
voir had lower chlorophyll a and higher Secchi depth
Hydrobiologia (2014) 740:115–135
values than those of Mediterranean reservoirs such as
eutrophic-hypertrophic El Gergal Reservoir (Moreno-
Ostos et al., 2008) and an eutrophic Sau Reservoir
(Becker et al., 2010). This could be consequence of
differences in physicochemical variables of those
reservoirs. Trophic state of Alleben limno-Reservoir
was mainly similar to Pareja limno-Reservoir (Moli-
na-Navarro et al., 2012, 2014) because they had
mainly similar pattern of physicochemical variables,
the mixing regime as a warm monomictic stratification
pattern, and climate in Mediterranean region. Besides,
anoxia in hypolimnion of Alleben Reservoir was
found in July and August 2012, which was also found
from Pareja limno-Reservoir (Molina-Navarro et al.,
2012). Besides, species of the genus Cyclotella was
predominant in the Alleben Reservoir, which was also
found in Paraja limno-Reservoir phytoplankton.
The abundance of phytoplankton assemblages in
the aquatic systems can be used as indicator of water
quality. Annex V of the WFD reported that ecological
status of phytoplankton in lentic ecosystems can be
assessed using biovolume and composition based on
metrics (Directive, 2000; EC, 2009; Poikane et al.,
2011; Phillips et al., 2013). The lowest PTI was found
as 0.25 in October 2012 (thermal stratification) and the
highest value was determined as 1.47 in November
2012 (began water mixing period). PTI indicated the
significant correlations with total phytoplankton bio-
volume, phosphate, chlorophyll a, and TSIChlo in
Alleben Reservoir for the whole set of samples.
Moderate PTI values (mean 0.738 ± 0.308) indicate
middle-grade ecological status of Alleben Reservoir.
The range of PTI values (-1.39 to 1.93) with different
color is illustrated geographically by Philips et al.
(2013). The ecological status of Alleben Reservoir
was found to be similar with status of deep Mediter-
ranean Reservoirs (Marchetto et al., 2009) and some
lakes in Europe (Philips et al., 2013). The high Q index
value (interval of 2.90–3.42) was found in Alleben
Reservoir during the water mixing period, whereas it
was lower within the stratification period (interval of
2.60–3.05). The water circulation (mixing vs. strati-
fication) could affect both physicochemical variables
and phytoplankton composition and biovolume with
season. Thus, this pattern also changed Q index and
the ecological status of Alleben Reservoir. This index
had significant correlations with chlorophyll a, phos-
phate, PTI, and phytoplankton biovolume in Alleben
Reservoir for the whole set of samples. The mean
127
Q index (2.91) indicated a medium ecological status of
Alleben Reservoir during the study period (Padisák
et al., 2006). Both PTI and Q indices had the strong
correlation with trophic state indicators for the total set
of samples (Fig. 3a–f). Aforementioned results sug-
gested that both PTI and Q indices could be an
appropriate metric to assess the ecological status of
Alleben Reservoir during study period. Suitability of
phytoplankton metric was also demonstrated in Med-
iterranean Reservoirs (Marchetto et al., 2009; Molina-
Navarro et al., 2014).
The mean ratio of Zmix/Zeu had 1.31 ± 0.79 m
changed monthly in Alleben Reservoir, which could
affect the phytoplankton dynamics in terms of their
assemblages and abundance. The Zmix/Zeu ratio could
be used to make quantitative predictions of phyto-
plankton periodicity since it provides sufficient infor-
mation about input of light, energy, and also nutrients,
which affected by the water circulation (mixing vs.
stratification) (Naselli-Flores and Barone, 2007; Ho-
yer et al., 2009; Becker et al., 2010). This ratio showed
the significant correlations with PTI (P \ 0.01,
r = 0.657), Q index (P \ 0.05, r = 0.590), and
phosphate (P \ 0.01, r = 0.628) in Alleben. The
water mixing regime could cause to the overturning
and upwelling of nutrients which increased dissolved
inorganic N and P values in the epilimnion of Alleben
Reservoir. This pattern caused to increase water
turbidity and decrease light availability, whereas the
long stratification period could increase light avail-
ability in the epilimnion. Thermal stratification could
also prevent the transfer of the hypolimnetic nutrients
to epilimnion, which could play a limiting factor for
phytoplankton growth. The Zmix/Zeu ratio and season-
ality of phytoplankton were driven by the water
circulation, in agreement with results of limno-
ecological studies in Mediterranean region (Naselli-
Flores and Barone, 2007; Hoyer et al., 2009; Becker
et al., 2010). Besides, impact of this ratio was also
reported in previous limno-ecological studies (Souza
et al., 2008; Becker et al., 2010; Zohary et al., 2010;
Naselli-Flores & Barone, 2011). Alleben limno-Res-
ervoir had retention time of 0.76 years, which was also
found in Lake Sanabria (Negro et al., 2000). It stated
that water depth and retention time are important
factors, affecting on physical characteristics (e.g.,
thermal stratification, Zmix/Zeu, etc.) of the reservoirs
(Straškraba, 1999; Naselli-Flores, 1999; Soares et al.,
2008). The retention time can influence the
123
128
longitudinal and the vertical mixing patterns in water
bodies (Straškraba, 1999; Soares et al., 2008). The
long water retention time plays an important role in the
low variability of the vertical pattern, which is
responsible for its important chemical and biological
features. High chlorophyll a values were determined
in the present study. This could be mainly responsible
for low water retention time (Soares et al., 2008).
Besides, this pattern can influence the stability of
environmental conditions, which can affect cyano-
bacteria biovolume (Straškraba, 1999; Negro et al.,
2000). Cyanobacteria had higher biovolume in Alle-
ben Reservoir during the summer period, which could
be favored by thermal stratification pattern. Mediter-
ranean reservoirs such as Lake Sanabria and Valpará-
iso Reservoir (Negro et al., 2000) and Marathonas
Reservoir (Katsiapi et al., 2011) had different reten-
tion times, which caused to be a key factor in seasonal
changes for physico-chemical variables and phyto-
plankton features. Previous limno-ecological studies
(Naselli-Flores, 1999; Padisák et al., 1999; Tolotti
et al., 2010; Katsiapi et al., 2011) retorted that
phytoplankton community assembly was influenced
by water stability and water retention time.
Phytoplankton seasonality and ecological
preferences
Relative importance of phytoplankton biovolume–
environmental variables relationship in Alleben Res-
ervoir cannot be resolved on the present data, but the
problem can be turned round, to an extent, by
analyzing the likely specific requirements of the
phytoplankton that dominate its plankton. Such anal-
yses are in their infancy as, in most cases, the
particular requirements of given phytoplankton
assemblages are not well known; however, compari-
sons with previous studies may provide strong general
patterns. The phytoplankton periodicity in Alleben
Reservoir, in terms of biovolume fluctuations and of
functional-group representation, had obvious similar-
ities to those reported for Mediterranean water bodies
(Salmaso, 2002; Becker et al., 2010; Molina-Navarro
et al., 2014). Phytoplankton species belong to func-
tional groups of A, D, E, J, LO, LM, MP, P, and Y as
descriptor were evaluated in phytoplankton composi-
tion of Alleben Reservoir. For this reservoir, func-
tional groups of phytoplankton were used as an
indicator of trophic state for the first time.
123
Hydrobiologia (2014) 740:115–135
Diatoms are good indicator of water trophic state
(Rott, 1991; Stoermer & Smol, 1999; Reynolds, 2006).
Alleben Reservoir had high annual mean biovolume of
diatoms in the phytoplankton biovolume, which was
also found in a Mediterranean Valparáıso Reservoir
(Negro et al., 2000). The dominant centric diatom
Cyclotella species was found in Alleben Reservoir
during the entire study period and had noteworthy
contribution to total phytoplankton biovolume. Cy-
clotella planctonica and C. iris preferred relatively
low P values as 16.38 ± 1.81 and 16.79 ± 2.28,
respectively (Table 5), supported by result of CCA
(Fig. 5). Oligotrophy of the ecosystem was supported
by some characteristic of the assemblage, like the
development of small Cyclotella species in summer
(Reynolds, 1997; Reynolds et al., 2002; Çelekli, 2006;
Tolotti et al., 2007; Berlinger & Sigee, 2010). However,
C. planctonica and C. iris had development activity
during thermal stratification and complete water circu-
lation in Alleben Reservoir. Indeed, CCA (Fig. 5)
indicated that both Cyclotella species (group B) had
wide tolerance to environmental factors during the
study period and was predominant in the Alleben
Reservoir phytoplankton biovolume. This group has
also been described as dominant in Mediterranean
water bodies (Moreno-Ostos et al., 2008, Hoyer et al.,
2009; Molina-Navarro et al., 2012). For this group, the
habitat template has been described as mesotrophic,
small- and medium-sized water bodies (Reynolds et al.,
2002, Padisák et al., 2009), which corresponds with the
characteristics of Alleben Reservoir. This situation was
also observed in a Mediterranean and warm monomic-
tic Paraja limno-Reservoir (Molina-Navarro et al.,
2012). Reynolds (2006) and Padisák et al. (2009) stated
that centric diatoms were one of the best-adapted algal
groups to turbulent and turbid systems. Cyclotella
species were reported for various trophic state ecosys-
tems such as oligo-mesotrophic hard water reservoirs
(Dası́ et al., 1998), mesotrophic Gölköy Reservoir
(Çelekli, 2006), and Mediterranean Marathonas Reser-
voir (Katsiapi et al., 2011). Previous limno-ecological
studies (Barbosa & Padisák, 2002; Souza et al., 2008;
Molina-Navarro et al., 2014) reported that atelomixis is
a mixing pattern in water column during stratification
periods, driven by the difference in day-night water
temperature. This pattern can affect entire water
column or the epilimnion as partial atelomixis. This
complex pattern could drive phytoplankton assemblage
in Alleben Reservoir during the summer (about 14°C
Hydrobiologia (2014) 740:115–135
differences between the daytime and nighttime periods)
in agreement with findings of Barbosa et al. (2011) for a
warm monomictic shallow tropical lake. Atelomixis
pattern was also evaluated in Mediterranean water
bodies (Naselli-Flores, 2003; Barbosa et al., 2011;
Katsiapi et al., 2011; Molina-Navarro et al., 2014).
Ecological relevance of this pattern was discussed in
detail by Barbosa & Padisák (2002). Hoyer et al. (2009)
reported that non-motile and non-buoyant phytoplank-
ton species such as Cyclotella are thought to sink into the
hypolimnion during thermal stratification. Atelomixis
could play significant role in preventing the sinking of
Cyclotella and other nonmotile algae from the epilim-
nion to the hypolimnion in Alleben Reservoir, but
further research is required to confirm this hypothesis.
The diatoms (especially species of Fragilaria) were
predominant in the spring periods, as they able to take
advantage of the available nutrient resources in turbulent
conditions. The spring and autumn phases of dominance
of F. biceps, followed by F. ulna and F. crotonensis
mirror the great seasonal contributions to algal biovo-
lume in Alleben Reservoir. Results of WA indicated that
F. biceps developed strongly in warm, circumneutral pH,
moderate nutrient, and hard waters (15.51 ± 4.99°C, pH
7.76 ± 0.55, 18.45 ± 2.65 lg l-1 PO4, 0.51 ± 0.17
mg l-1 NO3, 48.38 ± 15.43 mg l-1 Ca, and 8.20 ±
2.05 mg l-1 Mg). F. ulna preferred circumneutral pH
(pH 7.11 ± 0.38) in Alleben Reservoir (Table 5).
Indeed, WA and CCA indicated that Fragilaria species
had preference of higher PO4 value and nearly located
at spring months than those of other taxa in Alleben
Reservoir during the study period. Preference of
optimum pH for F. ulna in the present study was also
found for Synedra ulna (synonym of Fragilaria ulna)
in the stream (Bere & Tundisi, 2009). F. ulna had
important biovolume peaks in the spring and autumn,
when water mixing periods occurred with enriched
turbid water in Alleben Reservoir. Water mixing may
result in drifting of littoral diatoms to the plankton. This
species can be ascribed to the survival strategies of MP
functional group. The habitat template for this group is
typical of frequently stirred up and inorganically turbid
shallow lakes (Padisák et al., 2009), which corresponds
with the characteristics of Alleben Reservoir. This
diatom was reported from the artificial and modified
lakes in Italy (Tolotti et al., 2010). Fragilaria crotonen-
sis, had important biovolume peaks in the spring during
the water mixing period in Alleben limno-Reservoir, is
attributed to P functional group, whose habitat template is
129
typical of eutrophic epilimnia and species sensitive to
stratification (Reynolds et al., 2002; Padisák et al., 2009).
Fragilaria did not have an unusually high demand for
phosphorus or nitrogen (Reynolds, 2006) and some
regard it as a species having very low P requirements,
similar to those of a typical alpine diatom, but moderate
N requirements (Saros et al., 2005). Fragilaria biceps is
cosmopolitan species around the world, but its notewor-
thy contribution to phytoplankton biovolume has not
been found in the literature. F. biceps was found in
Alleben Reservoir during the entire study period and had
development activity during the complete water circula-
tion and thermal stratification. Results of CCA and WA
indicated that F. biceps preferred high phosphate value,
which was also found and related to phosphate variable in
a limnocrene type of Akkaya Spring (Çelekli &
Külköylüoğlu, 2007). The deductive approaches of
Reynolds et al. (2002), which separates the phytoplank-
ton species on basis of their morphological and physi-
ological properties, as influenced by ecological stressors
(biotic and abiotic factors), F. biceps (non-motile
microplankton) favored in eutrophic epilimnia of shallow
turbid waters including rivers, tolerant of flushing and
truncated photoperiods but sensitive to nutrient deple-
tion. Reynolds (1984) reported that negatively buoyant
algae are characterized by rapid sinking under calm
conditions of thermal stratification and require turbu-
lence to remain in suspension. This case with regard to
buoyancy of F. biceps in Alleben Reservoir could be
supported by the atelomixis pattern.
Among the chlorophyts, Tetraedron sp., ascribed to
functional group of J (Padisák et al., 2003, 2009), had
main biovolume peaks in May 2012, September 2012,
and May 2013, after the decreasing of F. biceps
biovolume. The habitat template for this group is
typical of shallow, mixed, and highly enriched
systems (including many low-gradient rivers) (Pad-
isák et al., 2009), which mainly corresponds with the
characteristics of Alleben Reservoir. As given in
Table 5, this species preferred warmer, lower P, and
softer waters (18.87 ± 3.93°C, 17.96 ± 2.94 lg l-1
PO4, 39.19 ± 13.43 mg l-1 Ca and 7.79 ± 2.30
mg l-1 Mg) than that of F. biceps. These results were
also confirmed by CCA (Fig. 5). Tetraedron species
was commonly found in Alleben Reservoir, which
also reported from Mediterranean Reservoirs such as
Marathonas Reservoir, Greece (Katsiapi et al., 2011),
Mediterranean reservoirs (Marchetto et al., 2009), and
Valparaı́so Reservoir, Spain (Negro et al., 2000).
123
130
The chrysophyte in the phytoplankton of Alleben
Reservoir, whose main representative is Dinobryon
divergens, had main biovolume peaks in the beginning
and ending of thermal stratification months. As
indicated in Table 5, D. divergens developed strongly
in warm, alkaline, hard water (18.38 ± 4.78°C, pH
7.9 ± 0.46, 45.93 ± 6.39 mg l-1 Ca and 9.24
± 1.08 mg l-1 Mg). This was intuitively remarkable,
given the oft-stated, long-accepted preference of
Dinobryon spp. for the cool oligotrophic waters
(Rawson, 1956; Rodhe et al., 1958; Çelekli, 2006).
Chrysophytes were the most important algal group in
oligotrophic Lake Saanajärvi, northern Finland (For-
sström et al., 2005), as they were reported in the
presence of high mountain lakes of Central Europe,
such as Lake Paione Superiore in Italy (Pugnetti &
Bettinetti 1999), in a small suburban Lake Strzeszyńs-
kie, Poland (Szela˛g-Wasielewska, 2006), and the
oligotrophic mountain lake, Laghetto Inferiore, in
Switzerland (Simona et al., 1999). Reynolds et al.
(2002) placed Dinobryon and many smaller chryso-
phytes in their functional Group E. The habitat
template for this group is typical of usually small,
shallow, base poor lakes or heterotrophic ponds
(Reynolds et al., 2002; Padisák et al., 2009), which
mainly attributed to the properties of Alleben Reser-
voir. Though principally associated with oligotrophic
lakes, where their life cycle and low proximal
phosphorus demands provide aids to their survival, it
was noted that algae of this group are generally absent
from calcareous lakes, yet do frequently occur in
calcareous ponds in which there is decomposition of
organic plant remains or some farm runoff. On the
other hand, Dinobryon sociale became briefly abun-
dant in the calcareous Lake Balaton, following
dredging operations that disturbed the bottom sedi-
ment (Reynolds et al., 1993). A capacity for mixotro-
phy (some chrysophytes, including Dinobryon, ingest
bacteria as an additional nutritive source to photo-
autotrophy: e.g., previous studies (Bird & Kalff, 1987;
Isaksson et al., 1999) may be important to the
ecological interpretation. The strong suggestion that
the chrysophytes were starved of carbon and were
unable to concentrate carbon from sources other than
carbon dioxide in solution has been verified through
exhaustive experiments (Saxby-Rouen et al., 1998).
The reputation of Dinobryon as an indicator of
oligotrophic conditions was conditioned not by a
preference for low phosphorus availability but an
123
Hydrobiologia (2014) 740:115–135
intolerance of competitors exhausting the carbon.
Lakes well buffered by bicarbonate also make it
difficult for Dinobryon to satisfy its carbon require-
ment. This being so, the restriction of Dinobryon to
soft water lakes ought to be inviolable, yet its seasonal
abundance in Alleben Reservoir is far from being an
isolated instance. Others include the karstic Akkaya
spring (Çelekli & Külköylüoğlu, 2007); the deep
mesotrophic Lake Zagłe˛bocze of Poland with alkaline
water (Solis, 2005); and in the alpine Piburger See in
Austria (Tolotti & Thies, 2002).
The dinoflagellate in Alleben Reservoir, Peridini-
um cinctum, showed its main biovolume peaks in the
early autumn and summer seasons, when the water
column thermal stratification was present. As given in
Table 5, this species preferred warm and slightly
alkaline water (19.31 ± 6.09°C and pH 8.01 ± 0.37),
which was also confirmed by CCA (Fig. 5). This
species was adapted to warm water and water strat-
ification, which is assigned to the association of Lo
functional group, which is related with summer
epilimnia in mesotrophic lakes (Reynolds et al.,
2002; Padisák et al., 2009). Peridinium species was
also reported from Mediterranean reservoirs (Mar-
chetto et al., 2009), and a shallow Torrens Lake in the
South Australia (Regel et al., 2004). Naselli-Flores
and Barone (2000) highlighted that dinophytes of the
genus Peridinium were among the most important
species in two (one natural and one artificial) meso-
trophic Sicilian lakes.
Among the crytophytes, Cryptomonas ovata was
found in Alleben Reservoir during the entire study
period and had higher biovolume than that of Plagio-
selmis nannoplanctica (mainly in spring and autumn).
Both small cryptophytes had no important contribution
to total phytoplankton biovolume of Alleben Reservoir.
Reynolds et al. (2002) and Padisák et al. (2009) reported
that the small cryptophytes, P. nannoplanctica and C.
ovata, were grouped in the X2 (typical of shallow meso-
eutrophic waters) and the Y (usually small and enriched
lakes) functional groups, respectively. Both taxa had
high biovolume during the mixing period in Alleben
Reservoir. Becker et al. (2010) reported that these
groups adapted to low light intensity, such as group Y in
a Mediterranean Reservoir.
Several limno-ecological studies regarding phyto-
plankton have been carried out in Mediterranean
region (Naselli-Flores, 2003; Moreno-Ostos et al.,
2008; Hoyer et al., 2009; Becker et al., 2010; Katsiapi
Hydrobiologia (2014) 740:115–135
et al., 2011; Molina-Navarro et al., 2014). Very rich
limnosystems are present in Mediterranean region,
although knowledge about ecology of the organisms
with long-term monitoring is generally rather poor
(Alvarez Cobelas et al., 2005). From that point, the
present study regarding phytoplankton or limno-
ecology in Alleben Reservoir is the first study of this
kind in the southeast of Turkey. The present study
covered 15 months and resulted that a part of limno-
logical investigations centered on the southeast region
of Turkey sets out to explain some distinctive features
of the phytoplankton of this Reservoir. Phytoplankton
biovolume temporally changed, and Cyclotella spe-
cies was found to be dominant group in Alleben
Reservoir. Nutrient dynamics and light availability
were mainly driven by the water circulation (stratifi-
cation vs. mixing) pattern, governing the phytoplank-
ton dynamics in Alleben Reservoir. This driving force
on phytoplankton was also found in Mediterranean
water bodies (Becker et al., 2010; Katsiapi et al., 2011;
Molina-Navarro et al., 2014). Ecological status of
phytoplankton in Alleben Reservoir was assessed
using PTI and Q indices in accordance with Annex V
of the WFD (Padisák et al., 2006; EC, 2009; Poikane
et al., 2011; Phillips et al., 2013). The national
assessment systems for phytoplankton in lakes and
reservoirs have been studied in many countries of
Europe, however, still lack metrics for phytoplankton
composition (Poikane, 2009, Birk et al. 2012). From
that point, the present study will be a contribution to
the usage of phytoplankton assemblages as a biolog-
ical metric in this region.
Conclusions
Alleben Reservoir was a warm monomictic charac-
teristic according to water circulation pattern. This
reservoir showed characteristic of meso-eutrophic
with respect to the chlorophyll a and Secchi depth
that it supported by criteria of OECD and the solution
of Carlson’s trophic state index. This study also
revealed that the suitability of phytoplankton biovo-
lume, chlorophyll a, phosphate, Secchi depth, PTI,
and Q index were evaluated for assessing the trophic
state and the ecological status of Alleben Reservoir in
accordance with the EU WFD, OECD, and Carlsons’
solution. A total of 76 counted species in Alleben
Reservoir belonging to 20 functional groups were
131
recorded during study period. Phytoplankton species
belong to the functional groups of A, D, E, J, LO, LM,
MP, P, and Y as descriptor were evaluated in
phytoplankton composition of Alleben Reservoir.
For this reservoir, functional groups of phytoplank-
ton were used as an indicator of trophic state for the
first time. The study confirmed the potential use of
the functional groups scheme of phytoplankton for
assessing the trophic state and ecological status, and
provided valuable and complementary information
on algal strategies, adaptations, and tolerances to
characterize and understand phytoplankton dynamics
in the reservoirs. Total phytoplankton biovolume
(9106 lm3 l-1) ranged between 64.3 in October
2012 (thermal stratification pattern) and 290.1 in
November 2012 (began water mixing period). Phy-
toplankton species; the diatom, especially C. plan-
ctonica, C. iris, and F. bicep; the dinoflagellate,
Peridinium cinctum; the chlorophyts Tetraedron sp.;
and the chrysophytes, Dinobryon divergens had
important contribution to the total biovolume. CCA
indicated that salinity, temperature, pH, conductiv-
ity, and phosphate were the most important variables
governing the seasonal succession of phytoplankton
species. Multivariate analyses indicated that Cyclo-
tella species and C. ovata were mainly found in
cooler water, while Peridinium species and C. hirun-
dinella preferred warmer water during study period.
Species of Fragilaria preferred higher PO4 value
than those of other phytoplankton taxa. Furthermore,
Cyclotella species were found in harder water,
comparing other phytoplankton taxa. From those
points, the present study regarding phytoplankton or
limno-ecology in Alleben Reservoir is the first study
of this kind in the South East of Turkey. Further
studies are needed to resolve some of the curious
biological features of warm monomictic Alleben
Reservoir that this investigation has revealed. The
use of multivariate analysis to explore the effects of
multiple environmental variables on the phytoplank-
ton is, demonstrably, a powerful means of explora-
tion of mechanisms and of isolation of the critical
determinants. The case for invoking the species-
specific biovolumes as an index of importance in the
plankton, together with the ascription of the main
components to functional groups, is claimed to
provide an important additional dimension in future
biomonitoring studies of the reservoir, lake, and
other water bodies.
123
132
Acknowledgements This research was supported by
TUBITAK (The Scientific and Technical Research Council of
Turkey) with the project No: 112Y002. Authors thank to
Scientific Research Projects Executive Council of University of
Gaziantep (FEF.12.01) and Gaziantep water and sewage
management (GASKI). Finally, we thank anonymous editor
and reviewers for valuable comments and suggestions on the
manuscript.
References
Abranthes, N., S. C. Antunes, M. J. Pereira & F. Gonçalves,
2006. Seasonal succession of cladocerans and phyto-
plankton and their interactions in a shallow eutrophic lake
(Lake Vela Portugal). Acta Oecologica-International
Journal of Ecology 29: 54–64.
Alvarez Cobelas, M., C. Rojo & D. G. Angeler, 2005. Medi-
terranean limnology: current status, gaps and the future.
Journal of Limnology 64(1): 13–29.
APHA AWWA, 1989. Standard methods for the examination of
water and wastewater. 17th ed, American Public Health
Association, Washington D.C.
Babanazarova, O. V. & O. A. Lyashenko, 2007. Inferring long-
term changes in the physical–chemical environment of the
shallow enriched Lake Nero from statistical and functional
analyses of its phytoplankton. Journal of Plankton
Research 29(9): 747–756.
Barbosa, F. A. R. & J. Padisák, 2002. The forgotten lake strat-
ification pattern: atelomixis, and its ecological importance.
Verhandlungen Internationaler Verein der Limnologie 28:
1385–1395.
Barbosa, L. G., P. M. M. Barbosa & F. A. R. Barbosa, 2011.
Vertical distribution of phytoplankton functional groups in
a tropical shallow lake: driving forces on a diel scale. Acta
Limnologica Brasiliensia 23: 63–73.
Becker, V., L. Caputo, J. Ordóñez, R. Marcé, J. Armengol, L.
O. Crossetti & V. L. M. Huszar, 2010. Driving factors of
the phytoplankton functional groups in a deep Mediterra-
nean reservoir. Water Research 44(11): 3345–3354.
Bere, T. & J. G. Tundisi, 2009. Weighted average regression and
calibration of conductivity and pH of benthic diatom
assemblages in streams influenced by urban pollution – São
Carlos/SP, Brazil. Acta Limnologica Brasiliensia 21(3):
317–325.
Berlinger, E. G. & D. C. Sigee, 2010. Freshwater Algae. Iden-
tification and use as Bioindicators, 1st ed. Wiley, London.
Bird, D. F. & J. Kalff, 1987. Algal phagotrophy: regulating
factors and importance relative to photosynthesis in Di-
nobryon (Chrysophyceae). Limnology and Oceanography
32: 277–284.
Birk, S., W. Bonne, A. Borja, S. Brucet, A. Courrat & S. Poi-
kane, 2012. Three hundred ways to assess Europe’s surface
waters: an almost complete overview of biological meth-
ods to implement the Water Framework Directive. Eco-
logical Indicators 18: 31–41.
Brettum, P., 1989. Alger som indikatorer pa vannkvalitet i
norske innsjǿer. NIVA Report, Planteplankton.
Carlson, R. E., 1977. A trophic state index for lakes. Limnology
and Oceanography 22(2): 361–369.
123
Hydrobiologia (2014) 740:115–135
Çelekli, A., 2006. Comparative Analysis of Seasonal Water
Quality Changes and Algae Potential between Lake Abant
and Lake Gölköy. Ph.D. Thesis, University of Abant İzzet
Baysal, Institute of Science.
Çelekli, A. & O. Külköylüoğlu, 2007. On the relationship
between ecology and phytoplankton composition in a
karstic spring (Çepni Bolu). Ecological Indicators 7:
497–503.
Dası́, M. J., M. R. Miracle, A. Camacho, J. M. Soria & E.
Vicente, 1998. Summer phytoplankton assemblages across
trophic gradients in hardwater reservoirs. Hydrobiologia
369/370: 27–43.
Dokulil, M. T. & K. Teubner, 2003. Eutrophication and resto-
ration of shallow lakes – the concept of stable equilibria
revisited. Hydrobiologia 506(509): 29–34.
Directive, 2000. Directive 2000/60/EC of the European parlia-
ment and of the council of 23 October 2000 establishing a
framework for community action in the field of water
policy. Official Journal of the European Communities 327:
1–72.
European Communities (EC), 2009. Water Framework Direc-
tive intercalibration technical report. Part 2. In Poikane, S.
(ed.), Lakes. European Commission, Joint Research Cen-
tre, Ispra.
Ettl, H., 1983. Chlorophyta I Phytomonadina. In Süßwasserflora
von Mitteleuropa. Band 6 Gustav Fischer Verlag Stuttgart.
Forsström, L., S. Sorvari & A. Korhola, 2005. Seasonality of
phytoplankton in subarctic Lake Saanajarvi in NW Finnish
Lapland. Polar Biology 28: 846–861.
Hall, R. I. & J. P. Smol, 1992. A weighted-averaging regression
and calibration model for inferring total phosphorus con-
centration from diatoms in British Columbia (Canada)
lakes. Freshwater Biology 27: 417–434.
Heinonen, P., 1980. Quantity and composition of phytoplankton
in Finnish inland waters. Publications of the Water
Research Institute 37: 1–91.
Hillebrand, H., C. D. Dürselen, D. Kirschtel, D. Polingher & T.
Zohary, 1999. Biovolume calculation for pelagic and
benthic microalgae. Journal of Phycology 35: 403–424.
Honti, M., V. Istvánovics & A. Osztoics, 2007. Stability and
change of phytoplankton communities in a highly dynamic
environment-the case of large, shallow Lake Balaton
(Hungary). Hydrobiologia 581: 225–240.
Horne, J. A. & C. R. Goldman, 1994. Limnology, 2nd ed.
McGraw–Hill Inc., New York.
Hoyer, A. B., E. Moreno-Ostos, J. Vidal, J. M. Blanco, R.
L. Palomino-Torres, A. Basanta, C. Escot & F. J. Rueda,
2009. The influence of external perturbations on the
functional composition of phytoplankton in a Mediterra-
nean reservoir. Hydrobiologia 636: 49–64.
Hutchinson, G. E., 1967. A Treatise on Limnology. Volume II;
Introduction to Lake Biology and the Limnoplankton.
Wiley, New York.
Isaksson, A., A. K. Bergström, P. Blomqvist & M. Jansson,
1999. Bacterial grazing by phagotrophic phytopflagellates
in a deep humic lake in northern Sweden. Journal of
Plankton Research 21(2): 247–268.
Istvánovic, V., M. Honti, A. Osztoics, H. M. Shafik, J. Padisák,
Y. Yacobi & W. Eckert, 2005. Continuous monitoring of
phytoplankton dynamics in Lake Balaton (Hungary) using
Hydrobiologia (2014) 740:115–135
on-line delayed fluorescence excitation spectroscopy.
Freshwater Biology 50: 1950–1970.
John, D. M., B. A. Whitton & J. A. Brook, 2002. The Freshwater
Algal Flora of the British Isles, 1st ed. Cambridge Uni-
versity Press, Cambridge.
Juggins, S. & C. F. J. ter Braak, 1992. CALIBRATE-Program
for species-environment calibration by (weighted averag-
ing) partial least squares regression. Environmental
Change Research Centre, University College London,
London.
Katsiapi, M., M. Moustaka-Gouni, E. Michaloudi & K.
A. Kormas, 2011. Phytoplankton and water quality in a
Mediterranean drinking-water reservoir (Marathonas Res-
ervoir, Greece). Environmental Monitoring and Assess-
ment 181: 563–575.
Komárek, J. & K. Anagnostidis, 1998. Cyanoprokaryota
Chroococcales. In Susswasserflora von Mitteleuropa.
Gustav Fisher, Jena.
Komárek, J. & B. Fott, 1983. Chlorophyceae (Grünalgen)
Ordnung: Chlorococcales. In Huber–Pestallozi – Das
Phytoplankton des Süßwassers Systematik und Biologie 7
Teil, 1 Hälfte E Schweizerbart‘sche Verlagsbuchhandlung,
Stuttgart.
Krammer, K. & H. Lange-Bertalot, 1991a. Bacillariophyceae. 3
Teil: Centrales, Fragilariaceae, Eunotiaceae. In Ettl,
H., J. Gerloff, H. Heynig & D. Mollenhauer (Hrsgb.),
Süßwasserflora von Mitteleuropa. Band 2. Fischer Verlag,
Stuttgart.
Krammer, K. & H. Lange-Bertalot, 1991b. Bacillariophyceae. 4
Teil: Achnanthaceae. Kritische Erganzungen zu Navicula
(Lineolatae) und Gomphonema. In Ettl, H., G. Gartner, J.
Gerloff, H. Heynig & D. Mollenhauer (eds), Süßwasserfl-
ora von Mitteleuropa. Band 2. Fischer Verlag, Stuttgart.
Krammer, K. & H. Lange–Bertalot, 1999a. Bacillariophyceae. 1
Teil: Naviculaceae. In Ettl, H., J. Gerloff, H. Heynig & D.
Mollenhauer (eds), Süßwasserflora von Mitteleuropa.
Band 2. Akademischer Verlag, Heidelberg, Berlin.
Krammer, K. & H. Lange–Bertalot, 1999b. Bacillariophyceae. 2
Teil: Bacillariaceae, Epithemiaceae, Surirellaceae. In Ettl,
H., J. Gerloff, H. Heynig & D. Mollenhauer (eds), Süß-
wasser-flora von Mitteleuropa. Band 2. Akademischer
Verlag, Heidelberg, Berlin.
Kruk, C., N. Mazzeo, G. Lacerot & C. S. Reynolds, 2002.
Classification schemes for phytoplankton: a local valida-
tion of a functional approach to the analysis of species
temporal replacement. Journal of Plankton Research 24(9):
901–912.
Leps, J. & P. Smilauer, 2003. Multivariate analysis of ecological
data using CANOCO Cambridge University Press,
Cambridge.
Marchetto, A., B. M. Padedda, M. A. Mariani, A. Lugliè & N.
Sechi, 2009. A numerical index for evaluating phyto-
plankton response to changes in nutrient levels in deep
Mediterranean reservoirs. Journal of Limnology 68:
106–121.
Molina-Navarro, E., A. Sastre-Merlı́n Martı́nez-Perez & D. M.
del Pozo, 2012. The limnological characteristics and zoo-
plankton community of a newly created site: the Pareja
Limno-reservoir. Limnetica 31(1): 95–106.
Molina-Navarro, E., S. Martı́nez-Perez, A. Sastre-Merlı́n, M.
Verdugo-Althöfer & J. Padisák, 2014. Phytoplankton and
133
suitability of derived metrics for assessing the ecological
status in a limno-reservoir, a Water Framework Directive
nondefined type of Mediterranean water body. Lake and
Reservoir Management 30: 46–62.
Moreno-Ostos, E., L. Cruz-Pizarro, A. Basanta & D. G. George,
2008. The spatial distribution of different phytoplankton
functional groups in a Mediterranean reservoir. Aquatic
Ecology 42: 115–128.
Naselli-Flores, L., 1999. Limnological aspects of Sicilian res-
ervoirs: a comparative, ecosystem approach. In Tundisi, J.
G. & M. Straškraba (eds), Theoretical Reservoir Ecology
and its Applications. Backhuys, Kerkwerve: 283–311.
Naselli-Flores, L., 2003. Man-made lakes in Mediterranean
semiarid climate: the strange case of Dr Deep Lake and Mr
Shallow Lake. Hydrobiologia 506–509: 13–21.
Naselli-Flores, L. & R. Barone, 2000. Phytoplankton dynamics
and structure: a comparative analysis in natural and man-
made water bodies of different tropic state. Hydrobiologia
438: 65–74.
Naselli-Flores, L. & R. Barone, 2007. Pluriannual morpholog-
ical variability of phytoplankton in a highly productive
Mediterranean reservoir (Lake Arancio, Southwestern
Sicily). Hydrobiologia 578: 87–95.
Naselli-Flores, L. & R. Barone, 2011. Invited review – fight on
plankton or, phytoplankton shape and size as adaptive tools
to get ahead in the struggle for life. Cryptogamie Algologie
32(2): 157–204.
Negro, A. I., C. De Hoyos & J. C. Vega, 2000. Phytoplankton
structure and dynamics in Lake Sanabria and Valparáıso
reservoir (NW Spain). Hydrobiologia 424: 25–37.
Padisák, J., J. Köhler & S. Hoeg, 1999. The effect of changing
flushing rates on development of late summer Aphani-
zomenon and Microcystis populations in a shallow lake,
Müggelsee, Berlin, Germany. In Tundisi, J. G. & M.
Straškraba (eds), Theoretical Reservoir Ecology and its
Applications. Backhuys, The Netherlands: 411–424.
Padisák, J., G. Borics, G. Fehér, I. Grigorszky, I. Oldal, A.
Schmidt & Z. Zámbóné-Doma, 2003. Dominant species,
functional assemblages and frequency of equilibrium phases
in late summer phytoplankton assemblages in Hungarian
small shallow lakes. Hydrobiologia 502: 157–168.
Padisák, J., G. Borics, I. Grigorszky & É. Soróczki-Pintér, 2006.
Use of phytoplankton assemblages for monitoring ecologi-
cal status of lakes within the Water Framework Directive:
the assemblage index. Hydrobiologia 553(1): 1–14.
Padisák, J., L. O. Crossetti & L. Naselli-Flores, 2009. Use and
misuse in the application of the phytoplankton functional
classification: a critical review with updates. Hydrobiolo-
gia 621: 1–19.
Padisák, J., E. Hajnal, L. Naselli-Flores, M. T. Dokulil, P. Nõges
& T. Zohary, 2010. Convergence and divergence in orga-
nization of phytoplankton communities under various
regimes of physical and biological control. Hydrobiologia
639: 205–220.
Phillips, G., A. Lyche-Solheim, B. Skjelbred, U. Mischke, S.
Drakare, G. Free, M. Järvinen, C. de Hoyos, G. Morabito,
S. Poikane, et al., 2013. A phytoplankton trophic index to
assess the status of lakes for the Water Framework Direc-
tive. Hydrobiologia 704: 75–95.
Poikane, S., M. V. D. Berg, J. Ortiz-Casas, G. Phillips, A.
L. Solheim, D. Tierney & G. Wolfram, 2009. Lake
123
134
assessment strategy in European Union (EU): case study of
European large lakes. Verh International Verein Limnol-
ogy 30: 1007–1012.
Poikane, S., M. van den Berg, S. Hellsten, C. de Hoyos, J. Ortiz-
Casas, K. Pall, R. Portielje, G. Phillips, A. L. Solheim, D.
Tierney, et al., 2011. Lake ecological assessment systems
and intercalibration for the European Water Framework
Directive: aims, achievements and further challenges.
Procedia Environmental Sciences 9: 153–168.
Popovsky, J. & L. A. Pfiester, 1990. Dinophyceae (Dinoflag-
ellida). In Süßwasserflora von Mitteleuropa. Band 6.
Gustav Fischer Verlag, Jena.
Pugnetti, A. & R. Bettinetti, 1999. Biomass and species structure
of the phytoplankton of a high mountain lake (Lake Paione
Superiore, Central Alps, Italy). Journal of Limnology 58:
127–130.
Rakocevic-Nedovic, J. & H. Hollert, 2005. Phytoplankton
community and chlorophyll a as trophic state indices of
Lake Skadar (Montenegro, Balkan). Environmental Sci-
ence and Pollution Research 12(3): 146–152.
Rawson, D. S., 1956. Algal indicators of trophic lake types.
Limnology and Oceanography 1: 18–25.
Reynolds, C. S., 1980. Phytoplankton assemblages and their
periodicity in stratifying lake system. Holarctic Ecology 3:
141–159.
Reynolds, C. S., 1984. Phytoplankton periodicity. Interactions
among form, function and environmental variability.
Freshwater Biology 14: 111–142.
Reynolds, C. S., 1997. Vegetation Processes in the Pelagic: A
Model for Ecosystem Theory. Ecology Institute, Olden-
dorf/ Luhe: 371.
Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cam-
bridge University Pres, Cambridge.
Reynolds, C. S., J. Padisák & I. Kóbor, 1993. A localized bloom
of Dinobryon sociale in Lake Balaton: Some implications
for the perception of patchiness and the maintenance of
species richness. Abstracta Botanica 17: 251–260.
Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S.
Melo, 2002. Towards a functional classification of the
freshwater phytoplankton, review. Journal of Plankton
Research 24(5): 417–428.
Rodhe, W., R. A. Vollenweider & A. Nauwerck, 1958. The
primary production and standing crop of phytoplankton. In
Buzzati-Traverso, A. A. (ed.), Perspectives in Marine
Biology. University of California Press, Berkeley.
Rott, E., 1981. Some results from phytoplankton counting in-
tercalibrations. Schweiz Z. Hydrologie 43: 34–62.
Rott, E., 1984. Phytoplankton as biological parameter for the
trophic characterization of lakes. Verhandlungen des In-
ternationalen Verein Limnologie 22: 1078–1085.
Rott, E., 1991. Methodological aspects and perspectives in the
use of periphyton for monitoring and protecting rivers. In
Whitton, B. A., E. Rott & G. Friedrich (eds), Use of Algae
for Monitoring Rivers. E. Rott, Institüt für Botanik, Univ.
Innsbruk, Innsbruk: 9–16.
Regel, R. H., J. D. Brookes & G. G. George, 2004. Vertical
migration, entrainment and photosynthesis of the fresh-
water dinoflagellate Peridinium cinctum in a shallow urban
lake. Journal of Plankton Research 26: 143–157.
123
Hydrobiologia (2014) 740:115–135
Salmaso, N., 2002. Ecological patterns of phytoplankton
assemblages in Lake Garda: seasonal, spatial and historical
features. Journal of Limnology 61(1): 95–115.
Salmaso, N. & J. Padisák, 2007. Morpho-functional groups and
phytoplankton development in two deep lakes (Lake
Garda, Italy and Lake Stechlin, Germany). Hidrobiologia
578: 97–112.
Saros, J. E., T. J. Michel, S. J. Interlandi & A. P. Wolfe, 2005.
Resource requirements of Asterionella formosa and
Fragilaria crotonensis in oligotrophic alpine lakes:
implications for recent phytoplankton community reorga-
nizations. Canadian Journal of Fisheries and Aquatic Sci-
ences 62: 1681–1689.
Saxby-Rouen, K. J., B. S. C. Leadbeater & C. S. Reynolds, 1998.
The relationship between the growth of Synura petersenii
(Synurophyceae) and the components of the dissolved
inorganic system. Phycologia 37: 467–477.
Simona, M., A. Barbieri, M. Veronesi, S. Malusardi & V.
Straskrábová, 1999. Seasonal dynamics of plankton in a
mountain lake in the Southern Alps (Laghetto Inferiore,
Switzerland). Journal of Limnology 58: 169–178.
Solis, M., 2005. Relationships between selected abiyotic vari-
ables and phytoplankton composition in deep mesotrophic
Lake Zaglebocze. Oceanological and Hydrobiological
Studies 19(4): 81–96.
Soares, M. C. S., M. M. Marinho, V. L. M. Huszar, C. W. C.
Branco & S. M. F. O. Azevedo, 2008. The effects of water
retention time and watershed features on the limnology of
two tropical reservoirs in Brazil. Lakes & Reservoirs:
Research and Management 13: 257–269.
Souza, M. B. G., C. F. A. Barros, F. Barbosa, É. Hajnal & J.
Padisák, 2008. Role of atelomixis in replacement of phy-
toplankton assemblages in Dom Helvécio Lake, South-
East Brazil. Hydrobiologia 6007: 211–224.
Stoermer, E. F. & J. P. Smol, 1999. The Diatoms: Applications
for the Environmental and Earth Sciences. Cambridge
University Press, Cambridge, UK.
Straškraba, M. 1999. Retention time as a key variable of res-
ervoir limnology. In Theoretical reservoir ecology and its
applications. In Tundisi, J. G. & M. Straskraba (eds),
International Institute of Ecology, Brazilian Academy of
Sciences and Backhuys Publishers, Leiden: 385–410.
Sun, J. & D. Liu, 2003. Geometric models for calculating cell
biovolume and surface area for phytoplankton. Journal of
Plankton Research 25: 1331–1346.
Szela˛g-Wasielewska, E., 2006. Trophic status of lake water
evaluated using phytoplankton community structure –
change after two decades. Polish Journal of Environmental
Studies 15(1): 139–144.
ter Braak, C. J. F., 1995. Ordination. In Jongman, R. H. G., C.
J. F. ter Braak & O. F. R. Van Tongeren (eds), Data Ana-
lysis in Community and Landscape Ecology. Cambridge
University Press, Cambridge.
ter Braak, C. J. F. & P. Smilauer, 1998. CANOCO Reference
Manual and User’s Guide to CANOCO for Windows
(Version 4). Center for Biometry, Wageningen.
Tolotti, M. & H. Thies, 2002. Phytoplankton community and
limnochemistry of Piburger See (Tyrol Austria) 28 years
after lake restoration. Journal of Limnology 61(1): 77–88.
Hydrobiologia (2014) 740:115–135
Tolotti, M., F. Corradini, A. Boscaini & D. Calliari, 2007.
Weather-driven ecology of planktonic diatoms in Lake
Tovel (Trentino, Italy). Hydrobiologia 578: 147–156.
Tolotti, M., A. Boscaini & N. Salmaso, 2010. Comparative
analysis of phytoplankton patterns in two modified lakes
with contrasting hydrological features. Aquatic Sciences
72: 213–226.
Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen
phytoplankton-methodik. Mitteilungen Internationale
Vereinigung Theoretische und Angewandte Limnologie
9: 1–38.
Vollenweider, R. A. & J. Kerekes, 1982. Eutrophication of
Waters, Monitoring, Assessment and Control. OECD
Cooperative Programme on Monitoring of Inland Waters
(Eutrophication Control). OECD, Paris.
View publication stats
135
Wehr, J. D. & R. G. Sheath, 2003. Freshwater Algae of North
America: Ecology and Classification. Academic Press, San
Jose.
Wetzel, R. G. & G. E. Likens, 2000. Limnological Analyses, 3rd
ed. Springer, Berlin.
Willén, E., 2000. Phytoplankton in water quality assessment-An
indicator concept. In Heinonen, P., G. Ziglio & A. Van der
Beken (eds), Hydrological and Limnological Aspects of
Lake Monitoring. Wiley, New York: 58–80.
Youngman, R. E., 1978. Measurement of Chlorophyll a Water
Research Center. Tech Rap Tr-82. Water Research Center,
New York.
Zohary, T., J. Padisák & L. Naselli-Flores, 2010. Phytoplankton
in the physical environment: beyond nutrients, at the end,
there is some light. Hydrobiologia 639: 261–269.
123