Professional Documents
Culture Documents
A26 Mediterranean Reservoir
A26 Mediterranean Reservoir
net/publication/266321786
CITATIONS READS
9 161
2 authors:
Some of the authors of this publication are also working on these related projects:
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.
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 Q indices may be appropriate phytoplankton metrics
Directive includes phytoplankton as one of the man- to assess the ecological status of the reservoir.
datory five biological indicators to be used to assess Changes in environmental gradients significantly
the ecological status of surface waters. The objective influenced the ecological preferences of species and
of the study was determination of ecological status and phytoplankton abundance in the reservoir. Canonical
ecological preferences of phytoplankton from April correspondence analysis (CCA) confirmed that phy-
2012 to June 2013, using multivariate approach in toplankton species were sensitive to environmental
Alleben Reservoir in the southeast Turkey. The variability, with the first two axes of CCA able to
reservoir showed a warm monomictic stratification explain 92.8% of the total variation and 37.1% of the
pattern (stratification in April–October 2012 vs. mix- cumulative percentage variance in the phytoplankton
ing in November 2012–March 2013). The reservoir assemblage structure. Most effective explanatory
was meso-eutrophic according to phosphorus, chloro- factors (e.g., salinity, conductivity, pH, and tempera-
phyll a, and transparence values. Phytoplankton ture) played significant role (P = 0.002) in the
biovolume reached remarkable peaks in autumn and seasonality of species.
spring. Phytoplankton species belong to functional
groups of A, D, E, J, LO, LM, MP, P, and Y as Keywords Mediterranean Reservoir Ecological
descriptor. Phytoplankton trophic index (PTI) and status Ecological preferences Functional group
assemblage index (Q) indicated the overall medium Phytoplankton
ecological status of Alleben Reservoir. PTI and
123
116 Hydrobiologia (2014) 740:115–135
gradual changes in the environment, generally those group of species to the same environmental variations,
brought about as a consequence of the interacting and these have provided a surprisingly sensitive means
activities of the organisms. The latter are thus of classifying both ecologically similar species and the
supposed to be autogenic and they comply with environmental conditions under which they flourish;
patterns understood to be those of succession (Rey- moreover, dynamics of these functional groups respond
nolds, 1980). Seasonal succession in the freshwater in similar ways to various sets of environmental
phytoplankton typically embodies a shift in domi- stressors (Reynolds et al., 2002; Padisák et al., 2006).
nance from small r-selected forms at their initiation to In this way, studies of phytoplankton and their season-
large K-selected organisms, often dominating toward ality are becoming a significant tool in limno-ecological
the end of stable phases of thermal stratification monitoring (Reynolds et al., 2002; Padisák et al., 2003;
(Reynolds, 1984). Unstable environmental conditions, Istvánovic et al., 2005; Padisák et al., 2006, 2009). It is
with full water circulation, relatively low light inten- sometimes difficult to differentiate the compounded
sity, and high of nutrients availability are also effects of several environmental factors operating
exploited by tolerant r-selected species. simultaneously, but the use of multivariate approaches
These seasonal changes in phytoplankton compo- allows some prediction to be made about the cumulative
sition are strongly influenced by intra-annual patterns impacts of multiple stressors on primary production and
and variations in the weather and in the associated trophic behavior (Kruk et al., 2002; Abranthes et al.,
physicochemical consequences (Hutchinson, 1967; 2006 Çelekli, 2006). Several long-term monitoring
Dokulil & Teubner, 2003; Reynolds, 2006; Zohary studies have invoked such methods to relate the
et al., 2010). However, even if the selection processes seasonality of the phytoplankton to contemporaneous
are broadly understood, prediction of dominance at the variations in the environment, and these have also
species level is generally difficult, save on the basis of helped to define better the habitat requirements of the
precedent. For much of the time, the phytoplankton algae (e.g., Forsström et al., 2005; Salmaso and Padisák,
constitutes a great diversity of species, present in 2007; Padisák et al., 2010). These approaches also
variable abundance (Wetzel & Likens, 2000; Abran- reinforce ecological classification of the phytoplankton
thes et al., 2006). Each may respond to temporal and species, the functional groupings of which interrelated
spatial variability in environmental factors, both biotic the ecologies, morphologies, and physiologies common
and abiotic (Horne & Goldman, 1994; Honti et al., to the members constituting each group, and which,
2007; Zohary et al., 2010), even though knowledge of arguably, underpin their seasonality and their dynamics
the ecological requirements of the organisms based on in particular water bodies (Reynolds et al., 2002).
long-term data is generally rather poor (Dokulil & The European Water Framework Directive (WFD)
Teubner, 2003; Alvarez Cobelas et al., 2005; Babana- outlines the ecological status of surface waters to be
zarova & Lyashenko, 2007; Naselli-Flores and Ba- assessed through the analysis of various characteristics
rone, 2007; Padisák et al., 2010). This is, in any case, a of aquatic flora and fauna (Directive, 2000; EC, 2009).
severe omission but it also misses the opportunity to Annex V of the WFD specifically requires that
use algal abundance and dynamics as a useful ecological status of phytoplankton in lentic ecosys-
biological tool for evaluating water quality (Rakoc- tems should be assessed using biovolume, composi-
evic-Nedovic & Hollert, 2005; Reynolds, 2006). tion, and chlorophyll a (EC, 2009; Poikane et al.,
Information about the composition, abundance, and 2011; Phillips et al., 2013). In many countries of
biovolume of phytoplankton is being applied to the Europe, the national assessment systems for phyto-
assessment of trophic condition in water bodies. Many plankton in lakes and reservoirs, however, still lack
studies of temporal and spatial distribution indicate that metrics for phytoplankton composition (Poikane,
the ecologies of specific algae are influenced by specific 2009, Birk et al., 2012).
environmental preferences (Reynolds, 1984; Hall & Several limno-ecological studies regarding phyto-
Smol, 1992). However, this information is still far from plankton have been carried out in Mediterranean
complete, and there remains a need for long-term data region (Naselli-Flores, 2003; Moreno-Ostos et al.,
that may better define species-specific ecological pref- 2008; Hoyer et al., 2009; Becker et al., 2010; Katsiapi
erences. Understanding has been assisted through et al., 2011; Molina-Navarro et al., 2014). Very rich
observations on the simultaneous dynamic reactions of limnosystems are present in Mediterranean region,
123
Hydrobiologia (2014) 740:115–135 117
although knowledge about ecology of the organisms Sport complex and restaurant are present near to the
with long-term monitoring is generally rather poor reservoir, whereas villas are located far away from the
(Alvarez Cobelas et al., 2005). From that point, the reservoir. Sport complex has a water treatment
present study regarding phytoplankton or limno- facility, whereas restaurant and villas have not. The
ecology in Alleben Reservoir is the first study of this characteristics of reservoir are maximum depth (Zmax):
kind in the southeast of Turkey. The present study, part 15.6 m, mean depth (Zmean): 7.5 m, surface area:
of a programme of limnological investigations cen- 0.34 km2, volume: 2.55 hm3, and catchment area:
tered on the southeast region of Turkey, sets out to 0.62 km2. Retention time was calculated theoretical as
explain some distinctive features of the phytoplankton 0.76 years and obtained from the General Directorate
of Alleben Reservoir. Here, main objectives of the of State Hydraulic Works (DSI, Turkey). The region is
study were as follows: (i) to determine phytoplankton characterized by a semiarid Mediterranean climate,
composition; (ii) to use phytoplankton metric to and water influx (Sacır creek) to the reservoir is
establish the ecological status of Alleben Reservoir, confined to the winter and spring months due to rainy
(iii) to analyze the relationship between biovolume of winter and spring followed by very dry summers.
phytoplankton species and limno-ecological charac- Between April 2012 and June 2013, water samples
teristics; and (iv) to estimate ecological preferences of were taken at monthly intervals at each of five stations
species for measured variables with using multivari- (Fig. 1), from just beneath of the surface for biological
able techniques, based on regular monitoring carried and physicochemical analyses. Vertical water samples
out in the reservoir for 15 months. 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
Materials and methods profile of water column during the study time and so to
predict the water mixing regime of this reservoir.
Alleben Reservoir (Fig. 1) is located at 939 m.a.s.l., Environmental variables were measured in situ: tem-
14 km the southwest Gaziantep City, and in the perature, oxygen concentration, saturation, conduc-
southeast Turkey (37°40 2900 N and 37°160 2000 E). The tivity, salinity, pH, redox potential, and total dissolved
reservoir was built on a wetland area in 1995s where solid (TDS), using an YSI–556 oxygen-temperature
water was aimed to be stored for the irrigation of meter from just beneath the surface in five stations and
agricultural uses, prevention of flooding, and recrea- the each meter of a depth profile in 5th station. Water
tional territory (Fig. 1). transparency was monthly measured using a 20-cm
123
118 Hydrobiologia (2014) 740:115–135
Secchi disk during the study period. Geographical data each taxon was multiplied by the corresponding
(elevation, latitude, and longitude) were read from a concentration to derive species-specific standing-crop
geographical positioning system. Atmospheric tem- volumes. Phytoplankton species were assigning into
perature and precipitation values were obtained from functional groups following the criteria of Reynolds
Gaziantep Meteorological Station, which is 10 km et al. (2002) and Padisák et al. (2003, 2006, 2009).
away from the southeast Alleben Reservoir. Species with high frequency and comprising more
Samples were stored in coolers with ice packs, than 10% of the total biovolume were considered to
pending transfer to the laboratory, where they were represent the significant presence of its ascribed
analyzed for chlorophyll content and selected chem- dominant group.
ical determinants. Chlorophyll a concentrations were Organization for Economic Cooperation and
determined by spectrophotometer after extraction in Development (OECD) criteria (Vollenweider & Kere-
90% methanol (Youngman, 1978). Analyses of chem- kes, 1982) and Carlson (1977) trophic state index
ical variables (N–NH4, N–NO3 N–NO2, P–PO4, and methods were utilized in order to calculate the trophic
SO4) and microbiological test (total coliform bacteria) state of reservoir based on values of chlorophyll a and
were carried out by standard methods (APHA Secchi disk depth. Besides, phytoplankton biovolume
AWWA, 1989). After Sartorius filtration technique, was used to assess the trophic state of reservoir.
chemical analyses of water samples were done by use Phytoplankton trophic index (PTI) and phytoplank-
of ion chromatography (Thermo Scientific Dionex ton assemblage index (Q) were used to assess the
ICS-5000, HPIC system). Heavy metals were ana- status of Alleben Reservoir according to the Water
lyzed using inductively coupled plasma-optical emis- Framework Directive. PTI value was calculated by the
sion spectrometry (ICP-OES, Perkin-Elmer, Optima use of following equation (Eq. 1) from the proportion
2100 DV). Water samples were incubated for 5 days at taxa corresponding to total biovolume (Philips et al.,
20°C in a dark place, in order to determine biological 2013).
oxygen demand (BOD5) (APHA, 1989). Turbidity of Pn
water was measured nephelometrically and expressed j¼1 aj sj
PTI ¼ Pn ; ð1Þ
in NTU. The taxonomic keys (Ettl, 1983; Komárek & j¼1 aj
Fott, 1983; Popovsky & Pfiester, 1990; Krammer &
where aj is proportion of jth taxon in the sample and sj
Lange-Bertalot, 1991a, b; Komárek & Anagnostidis,
is the optimum of jth taxon in the sample.
1998; Krammer & Lange-Bertalot, 1999a, b; John
The assemblage index (Q index) values were
et al., 2002; Wehr & Sheath, 2003) were consulted to
determined by following an equation (Eq. 2) proposed
assist phytoplankton identification. Identification of
by Padisák et al. (2006) from the proportion taxa
phytoplankton taxa was carried out by the use of
corresponding to total biovolume.
Olympus light microscope (Olympus BX53) attached
DP73 model digital camera with imaging software X
n
123
Hydrobiologia (2014) 740:115–135 119
surface area. Five levels of classification for the negligible biovolume value (\1% of total biovolume)
Q index were used as 0–1, poor ecological status; throughout the study were not taken in analyses.
1–2, tolerable; 2–3, medium; 3–4, good; and 4–5:
excellent.
Pearson’s correlation was used to test the relation- Results
ships among the environmental variables. Besides, this
test was also used to evaluate the correlations among Physicochemical and limnological variables
PTI, Q index, biovolume, chlorophyll a, phosphate,
Secchi depth, and Carlson’s trophic state. Canonical Physicochemical variables are given in Table 1. The
correspondence analysis (CCA), a direct gradient ana- water in Alleben Reservoir was slightly basic; pH
lysis technique, was used to elucidate the relationship readings ranged between 6.68 and 8.72 (mean
between predictor variables (environmental factors) 7.88 ± 0.51). Phosphate (PO4–P) varied seasonally
and the response variables (phytoplankton species) in with high values during complete water circulation,
the reservoir. Following ter Braak & Smilauer (1998), but it was observed to fall to concentrations
unimodal response models were employed for the (13.78 lg l-1) in October 2012. Among nitrogen
ordination of analyses along long gradients. Environ- species, ammonium (NH4–N) reached high values in
mental variables were transformed (ln (x ? 1), except the autumn–winter period, while nitrate (NO3–N) fell
for pH) to reduce skewness (ter Braak & Smilauer, from 0.83 mg l-1 in the winter to 0.32 mg l-1 in the
1998). For statistical analysis of data, all taxa over 1% summer. Minimum and maximum conductivities (EC)
of total phytoplankton biovolume, which corresponded of 278.0 and 414.0 lS cm-1 were noted in September
to the abundant species, were considered (ter Braak, 2012 and May 2013, respectively.
1995). The significance of environmental variables to Water thermal structure (Fig. 2a) by the depth
explain the variance of species data in CCA was tested distribution of isotherms relative to the surface season-
using forward selection of Monte Carlo simulations ally changed during the study period. The reservoir was
with 499 unrestricted permutations. Significant vari- thermally stratified between April and October in 2012.
ables at P \ 0.01 were performed for CCA analysis. The full circulation period usually begins in November
Thus, CCA analysis included 17 species of phyto- 2012 and ends in March 2013. The distribution of
plankton, 8 environmental variables, and 15 sampling dissolved oxygen concentration is tabulated in Table 1;
time (months) as supplementary variables. Seventy- readings ranged from 0.98 to 13.85 mg l-1, decreasing
five of sampling data (5 stations 9 15 months) were especially in the summer hypolimnion (Fig. 2b). Mean
carried out for CCA analysis. The program CANOCO ratio of mixing depth to euphotic depth (Zmix/Zeu) had
was used for the ordination analyses (ter Braak & 1.31 ± 0.79 m and increased in the autumn–winter
Smilauer, 1998; Leps & Smilauer, 2003). Weighted period. Significant variation in this ratio among seasons
averaging regression of CALIBRATE program (Jug- was found (P \ 0.05).
gins & ter Braak, 1992) was used to estimate species
optima (uk) and tolerance (tk) levels for environmental Trophic state and ecological status
variables. Objective of calibration is to estimate values
of environmental descriptors on the basis of species Value of chlorophyll a was generally higher in the
composition. For this purpose, weighted averaging spring and late autumn, but fell to low values in the
method is commonly used for the estimates of species summer and early autumn. This variable changed
optima in relation to selected environmental gradient. monthly from 4.98 to 23.50 lg l-1 for October 2012
Weighted-average metrics assess only a single pres- and November 2012, respectively. Total phytoplank-
sure (e.g., nutrients) or related pressures of environ- ton biovolume (9106 lm3 l-1) varied between 64.3
mental factors on organisms. Besides, calibration is and 290.1 for October 2012 and November 2012,
also one of the steps used in more complicated respectively. Water transparence changed between
analyses, such as ordination methods (Leps & Smil- 1.10 m and 3.32 m (mean 1.93 ± 0.49 m). The res-
auer, 2003). Some phytoplankton species comprising ervoir was meso-eutrophic according to phosphorus,
only its one occurrence (rare species) and having chlorophyll a, and transparence values, whereas it was
123
120 Hydrobiologia (2014) 740:115–135
oligotrophic state according to value of total phyto- Zmix/Zeu ratio (P \ 0.05, r = 0.590). Plots of indices
plankton biovolume (Table 2). Value of PTI varied vs. phytoplankton biovolume, phosphate, and chloro-
from 0.25 to 1.47 for October 2012 and November phyll a are given in Fig. 3a–f. Results indicated that
2012, respectively. PTI was positively correlated with both indices had the strong regression with aforemen-
phytoplankton biovolume (P \ 0.01, r = 0.758), PO4 tioned trophic state indicators for the total set of
(P \ 0.01, r = 0.881), and chlorophyll a (P \ 0.01, samples.
r = 0.793). The F weights for each functional group
identified appear in Table 3. The assemblage index (Q Seasonality of phytoplankton
index) ranged from 2.60 to 3.42 (mean 2.91) during the
study period. This indicated a medium ecological With regard to the counts of phytoplankton, a total of
status of Alleben Reservoir during the study period. 76 species in Alleben Reservoir belonging to 20
Q index was positively correlated with chlorophyll functional groups were recorded during study period
a (P \ 0.01, r = 0.731), PO4 (P \ 0.01, r = 0.860), (Appendix 1—Supplementary Material). Nine func-
phytoplankton biovolume (P \ 0.05, r = 0.542), and 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 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
123
122 Hydrobiologia (2014) 740:115–135
Fig. 3 PTI vs. (a) total phytoplankton biovolume, (b) chloro- Fig. 3 continued
phyll a, and (c) PO4. Q index vs. (d) total phytoplankton
biovolume, (e) chlorophyll a, and (f) PO4
spring (Fig. 4a). Total phytoplankton biovolume
found as descriptor and were consequently evaluated (9106 lm3 l-1) ranged between 64.3 and 290.1 (mean
in phytoplankton composition of Alleben (Table 3). 184.1 ± 15.2). The lowest total biovolume was found
Temporal variations in the algal biovolume are plotted in October 2012, while the highest value was deter-
in Fig. 4a. Phytoplankton biovolume showed temporal mined in November 2012 (began water mixing
variation and had remarkable peaks in autumn and period).
123
Hydrobiologia (2014) 740:115–135 123
Relative contributions of phytoplankton species to F. biceps strongly developed in April 2012 and 2013,
total biovolume are given in Fig. 4b. The diatom while the chlorophyts whose main representative is
species in the reservoir were usually found during the Tetraedron sp. has high biovolume peaks in May
entire study period. Phytoplankton species; the dia- 2012, September 2012, and May 2013. The dinofla-
tom, especially Cyclotella planctonica, C. iris, and gellate P. cinctum had remarkable peaks in June 2012,
Fragilaria biceps (for taxonomic authorities, see September 2012, and June 2013, while the chryso-
Appendix 1—Supplementary Material); the dinofla- phytes, dominated by D. divergens, developed in
gellate, Peridinium cinctum; the chlorophyts Tetrae- November 2012. During study period, other species
dron sp.; and the chrysophytes, Dinobryon divergens given in Fig 4b such as Fragilaria crotonensis,
had important contribution to the total biovolume. Fragilaria construens, Fragilaria ulna, Scenedesmus
Both mentioned Cyclotella species were major frac- communis, Pediastrum boryanum, Pediastrum duplex,
tions of biovolume value during thermal stratification Mougeotia parvula, Chlamydomonas lapponica, Pla-
and complete water circulation in Alleben Reservoir. gioselmis nannoplanctica, Peridiniopsis cunningtonii,
123
124 Hydrobiologia (2014) 740:115–135
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
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 Hydrobiologia (2014) 740:115–135
most frequently occurring species in Alleben Reser- phytoplankton growth could be determined in this
voir. Cyclotella species and C. ovata were mainly period due to consuming available phosphate by
found in cooler water, while Peridinium species and phytoplankton. Effect of mixing regime on availability
C. hirundinella preferred warmer water during study of the light and nutrients was observed in Mediterra-
period. Species of Fragilaria preferred higher PO4 nean water bodies as Sau Reservoir (Becker et al.,
value than those of other phytoplankton taxa. Further- 2010) and Pareja limno-Reservoir (Molina-Navarro
more, Cyclotella species were found in harder water, et al., 2014). Alleben Reservoir had a low transparency
comparing other phytoplankton taxa. (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
Discussion summer and early autumn. The overturning and
upwelling of the hypolimnetic nutrients through the
Physicochemical and limnological characteristics mixing regime in the reservoir could increase phyto-
plankton biovolume and chlorophyll-a and decrease
Temporal changes in the water column movements in Secchi depth.
lentic systems are one of the main environmental
forces (Reynolds, 1984; Barbosa & Padisák, 2002; Trophic state and ecological status
Reynolds, 2006). It is known that heat in aquatic
ecosystems had two physical functions as establish of Alleben Reservoir showed characteristic of meso-
thermal stratification and water mixing. Absorption of eutrophic (Table 2) with respect to the chlorophyll
solar energy by the water bodies seasonally changed, a and Secchi depth that it supported by criteria of
which caused to the water circulation. Four seasons are OECD (Vollenweider & Kerekes, 1982) and the
observed in Mediterranean region, so air temperature solution of Carlson’s Trophic State Index (TSI)
is mainly high and photoperiod is long in period of the (Carlson, 1977). Phytoplankton organisms give sensi-
between late spring and earlier autumn. This Medi- tive responses to the changes of water quality
terranean climate can undergo the long stratification (Hutchinson, 1967; Reynolds, 1984; Willen, 2000;
period in water bodies. Water circulation, stratification EC, 2000). For this reason, Willen (2000) presented
in April–October 2012 vs. mixing in November 2012– that phytoplankton biovolume as indicators for assess-
March 2013, indicated that Alleben Reservoir was ing the links between phytoplankton and the environ-
warm monomictic characteristic. Same water circula- ment can be used to evaluate water quality. With
tion (stratification vs. mixing) pattern was also found regard to phytoplankton biovolume, Alleben Reser-
for several reservoirs in the Mediterranean region such voir conformed to the maxima typical (Brettum,
as Sau Reservoir (Becker et al., 2010), El Gergal 1989), levels in mid-summer (Heinonen, 1980) and
Reservoir (Moreno-Ostos et al., 2008; Hoyer et al., the basis of the annual average of phytoplankton
2009), and Pareja limno-Reservoir (Molina-Navarro biovolume (Rott, 1984) were also similar to those said
et al., 2014). Reynolds (2006) reported that phyto- to typify oligotrophic systems (Table 2). Total phyto-
plankton growth is mainly related to availabilities of plankton biovolume could be limited due to the hard
light and nutrients, which driven by the mixing water of reservoir. Cyanobacterial biovolume (\1%)
regime. The mixing regime in the present study not had no significant contribution to total phytoplankton
only affected physicochemical variables (e.g., light biovolume in Alleben Reservoir. EC (2009) reported
and nutrients), but also affected phytoplankton that species of cyanobacteria associated with eutro-
dynamics (e.g., their seasonality based on the avail- phic conditions were considered for the percent
ability of growth-limiting resources and buoyance). contribution of cyanobacteria as a metric. Phytoplank-
The mixing period in the winter and the premixing in ton biovolume and Secchi depth values in Alleben
the late autumn in Alleben limno-Reservoir could Reservoir was similar to an oligo-mesotrophic Med-
affect light availability which could play a limiting iterranean Pareja limno-Reservoir (Molina-Navarro
factor for phytoplankton growth. The long stratifica- et al., 2012, 2014); however, Alleben Reservoir had
tion period in this reservoir could led to high light higher chlorophyll a value. Whereas, Alleben Reser-
availability in the epilimnion, whereas P-limitation for voir had lower chlorophyll a and higher Secchi depth
123
Hydrobiologia (2014) 740:115–135 127
values than those of Mediterranean reservoirs such as Q index (2.91) indicated a medium ecological status of
eutrophic-hypertrophic El Gergal Reservoir (Moreno- Alleben Reservoir during the study period (Padisák
Ostos et al., 2008) and an eutrophic Sau Reservoir et al., 2006). Both PTI and Q indices had the strong
(Becker et al., 2010). This could be consequence of correlation with trophic state indicators for the total set
differences in physicochemical variables of those of samples (Fig. 3a–f). Aforementioned results sug-
reservoirs. Trophic state of Alleben limno-Reservoir gested that both PTI and Q indices could be an
was mainly similar to Pareja limno-Reservoir (Moli- appropriate metric to assess the ecological status of
na-Navarro et al., 2012, 2014) because they had Alleben Reservoir during study period. Suitability of
mainly similar pattern of physicochemical variables, phytoplankton metric was also demonstrated in Med-
the mixing regime as a warm monomictic stratification iterranean Reservoirs (Marchetto et al., 2009; Molina-
pattern, and climate in Mediterranean region. Besides, Navarro et al., 2014).
anoxia in hypolimnion of Alleben Reservoir was The mean ratio of Zmix/Zeu had 1.31 ± 0.79 m
found in July and August 2012, which was also found changed monthly in Alleben Reservoir, which could
from Pareja limno-Reservoir (Molina-Navarro et al., affect the phytoplankton dynamics in terms of their
2012). Besides, species of the genus Cyclotella was assemblages and abundance. The Zmix/Zeu ratio could
predominant in the Alleben Reservoir, which was also be used to make quantitative predictions of phyto-
found in Paraja limno-Reservoir phytoplankton. plankton periodicity since it provides sufficient infor-
The abundance of phytoplankton assemblages in mation about input of light, energy, and also nutrients,
the aquatic systems can be used as indicator of water which affected by the water circulation (mixing vs.
quality. Annex V of the WFD reported that ecological stratification) (Naselli-Flores and Barone, 2007; Ho-
status of phytoplankton in lentic ecosystems can be yer et al., 2009; Becker et al., 2010). This ratio showed
assessed using biovolume and composition based on the significant correlations with PTI (P \ 0.01,
metrics (Directive, 2000; EC, 2009; Poikane et al., r = 0.657), Q index (P \ 0.05, r = 0.590), and
2011; Phillips et al., 2013). The lowest PTI was found phosphate (P \ 0.01, r = 0.628) in Alleben. The
as 0.25 in October 2012 (thermal stratification) and the water mixing regime could cause to the overturning
highest value was determined as 1.47 in November and upwelling of nutrients which increased dissolved
2012 (began water mixing period). PTI indicated the inorganic N and P values in the epilimnion of Alleben
significant correlations with total phytoplankton bio- Reservoir. This pattern caused to increase water
volume, phosphate, chlorophyll a, and TSIChlo in turbidity and decrease light availability, whereas the
Alleben Reservoir for the whole set of samples. long stratification period could increase light avail-
Moderate PTI values (mean 0.738 ± 0.308) indicate ability in the epilimnion. Thermal stratification could
middle-grade ecological status of Alleben Reservoir. also prevent the transfer of the hypolimnetic nutrients
The range of PTI values (-1.39 to 1.93) with different to epilimnion, which could play a limiting factor for
color is illustrated geographically by Philips et al. phytoplankton growth. The Zmix/Zeu ratio and season-
(2013). The ecological status of Alleben Reservoir ality of phytoplankton were driven by the water
was found to be similar with status of deep Mediter- circulation, in agreement with results of limno-
ranean Reservoirs (Marchetto et al., 2009) and some ecological studies in Mediterranean region (Naselli-
lakes in Europe (Philips et al., 2013). The high Q index Flores and Barone, 2007; Hoyer et al., 2009; Becker
value (interval of 2.90–3.42) was found in Alleben et al., 2010). Besides, impact of this ratio was also
Reservoir during the water mixing period, whereas it reported in previous limno-ecological studies (Souza
was lower within the stratification period (interval of et al., 2008; Becker et al., 2010; Zohary et al., 2010;
2.60–3.05). The water circulation (mixing vs. strati- Naselli-Flores & Barone, 2011). Alleben limno-Res-
fication) could affect both physicochemical variables ervoir had retention time of 0.76 years, which was also
and phytoplankton composition and biovolume with found in Lake Sanabria (Negro et al., 2000). It stated
season. Thus, this pattern also changed Q index and that water depth and retention time are important
the ecological status of Alleben Reservoir. This index factors, affecting on physical characteristics (e.g.,
had significant correlations with chlorophyll a, phos- thermal stratification, Zmix/Zeu, etc.) of the reservoirs
phate, PTI, and phytoplankton biovolume in Alleben (Straškraba, 1999; Naselli-Flores, 1999; Soares et al.,
Reservoir for the whole set of samples. The mean 2008). The retention time can influence the
123
128 Hydrobiologia (2014) 740:115–135
longitudinal and the vertical mixing patterns in water Diatoms are good indicator of water trophic state
bodies (Straškraba, 1999; Soares et al., 2008). The (Rott, 1991; Stoermer & Smol, 1999; Reynolds, 2006).
long water retention time plays an important role in the Alleben Reservoir had high annual mean biovolume of
low variability of the vertical pattern, which is diatoms in the phytoplankton biovolume, which was
responsible for its important chemical and biological also found in a Mediterranean Valparáıso Reservoir
features. High chlorophyll a values were determined (Negro et al., 2000). The dominant centric diatom
in the present study. This could be mainly responsible Cyclotella species was found in Alleben Reservoir
for low water retention time (Soares et al., 2008). during the entire study period and had noteworthy
Besides, this pattern can influence the stability of contribution to total phytoplankton biovolume. Cy-
environmental conditions, which can affect cyano- clotella planctonica and C. iris preferred relatively
bacteria biovolume (Straškraba, 1999; Negro et al., low P values as 16.38 ± 1.81 and 16.79 ± 2.28,
2000). Cyanobacteria had higher biovolume in Alle- respectively (Table 5), supported by result of CCA
ben Reservoir during the summer period, which could (Fig. 5). Oligotrophy of the ecosystem was supported
be favored by thermal stratification pattern. Mediter- by some characteristic of the assemblage, like the
ranean reservoirs such as Lake Sanabria and Valpará- development of small Cyclotella species in summer
iso Reservoir (Negro et al., 2000) and Marathonas (Reynolds, 1997; Reynolds et al., 2002; Çelekli, 2006;
Reservoir (Katsiapi et al., 2011) had different reten- Tolotti et al., 2007; Berlinger & Sigee, 2010). However,
tion times, which caused to be a key factor in seasonal C. planctonica and C. iris had development activity
changes for physico-chemical variables and phyto- during thermal stratification and complete water circu-
plankton features. Previous limno-ecological studies lation in Alleben Reservoir. Indeed, CCA (Fig. 5)
(Naselli-Flores, 1999; Padisák et al., 1999; Tolotti indicated that both Cyclotella species (group B) had
et al., 2010; Katsiapi et al., 2011) retorted that wide tolerance to environmental factors during the
phytoplankton community assembly was influenced study period and was predominant in the Alleben
by water stability and water retention time. Reservoir phytoplankton biovolume. This group has
also been described as dominant in Mediterranean
Phytoplankton seasonality and ecological water bodies (Moreno-Ostos et al., 2008, Hoyer et al.,
preferences 2009; Molina-Navarro et al., 2012). For this group, the
habitat template has been described as mesotrophic,
Relative importance of phytoplankton biovolume– small- and medium-sized water bodies (Reynolds et al.,
environmental variables relationship in Alleben Res- 2002, Padisák et al., 2009), which corresponds with the
ervoir cannot be resolved on the present data, but the characteristics of Alleben Reservoir. This situation was
problem can be turned round, to an extent, by also observed in a Mediterranean and warm monomic-
analyzing the likely specific requirements of the tic Paraja limno-Reservoir (Molina-Navarro et al.,
phytoplankton that dominate its plankton. Such anal- 2012). Reynolds (2006) and Padisák et al. (2009) stated
yses are in their infancy as, in most cases, the that centric diatoms were one of the best-adapted algal
particular requirements of given phytoplankton groups to turbulent and turbid systems. Cyclotella
assemblages are not well known; however, compari- species were reported for various trophic state ecosys-
sons with previous studies may provide strong general tems such as oligo-mesotrophic hard water reservoirs
patterns. The phytoplankton periodicity in Alleben (Dası́ et al., 1998), mesotrophic Gölköy Reservoir
Reservoir, in terms of biovolume fluctuations and of (Çelekli, 2006), and Mediterranean Marathonas Reser-
functional-group representation, had obvious similar- voir (Katsiapi et al., 2011). Previous limno-ecological
ities to those reported for Mediterranean water bodies studies (Barbosa & Padisák, 2002; Souza et al., 2008;
(Salmaso, 2002; Becker et al., 2010; Molina-Navarro Molina-Navarro et al., 2014) reported that atelomixis is
et al., 2014). Phytoplankton species belong to func- a mixing pattern in water column during stratification
tional groups of A, D, E, J, LO, LM, MP, P, and Y as periods, driven by the difference in day-night water
descriptor were evaluated in phytoplankton composi- temperature. This pattern can affect entire water
tion of Alleben Reservoir. For this reservoir, func- column or the epilimnion as partial atelomixis. This
tional groups of phytoplankton were used as an complex pattern could drive phytoplankton assemblage
indicator of trophic state for the first time. in Alleben Reservoir during the summer (about 14°C
123
Hydrobiologia (2014) 740:115–135 129
differences between the daytime and nighttime periods) typical of eutrophic epilimnia and species sensitive to
in agreement with findings of Barbosa et al. (2011) for a stratification (Reynolds et al., 2002; Padisák et al., 2009).
warm monomictic shallow tropical lake. Atelomixis Fragilaria did not have an unusually high demand for
pattern was also evaluated in Mediterranean water phosphorus or nitrogen (Reynolds, 2006) and some
bodies (Naselli-Flores, 2003; Barbosa et al., 2011; regard it as a species having very low P requirements,
Katsiapi et al., 2011; Molina-Navarro et al., 2014). similar to those of a typical alpine diatom, but moderate
Ecological relevance of this pattern was discussed in N requirements (Saros et al., 2005). Fragilaria biceps is
detail by Barbosa & Padisák (2002). Hoyer et al. (2009) cosmopolitan species around the world, but its notewor-
reported that non-motile and non-buoyant phytoplank- thy contribution to phytoplankton biovolume has not
ton species such as Cyclotella are thought to sink into the been found in the literature. F. biceps was found in
hypolimnion during thermal stratification. Atelomixis Alleben Reservoir during the entire study period and had
could play significant role in preventing the sinking of development activity during the complete water circula-
Cyclotella and other nonmotile algae from the epilim- tion and thermal stratification. Results of CCA and WA
nion to the hypolimnion in Alleben Reservoir, but indicated that F. biceps preferred high phosphate value,
further research is required to confirm this hypothesis. which was also found and related to phosphate variable in
The diatoms (especially species of Fragilaria) were a limnocrene type of Akkaya Spring (Çelekli &
predominant in the spring periods, as they able to take Külköylüoğlu, 2007). The deductive approaches of
advantage of the available nutrient resources in turbulent Reynolds et al. (2002), which separates the phytoplank-
conditions. The spring and autumn phases of dominance ton species on basis of their morphological and physi-
of F. biceps, followed by F. ulna and F. crotonensis ological properties, as influenced by ecological stressors
mirror the great seasonal contributions to algal biovo- (biotic and abiotic factors), F. biceps (non-motile
lume in Alleben Reservoir. Results of WA indicated that microplankton) favored in eutrophic epilimnia of shallow
F. biceps developed strongly in warm, circumneutral pH, turbid waters including rivers, tolerant of flushing and
moderate nutrient, and hard waters (15.51 ± 4.99°C, pH truncated photoperiods but sensitive to nutrient deple-
7.76 ± 0.55, 18.45 ± 2.65 lg l-1 PO4, 0.51 ± 0.17 tion. Reynolds (1984) reported that negatively buoyant
mg l-1 NO3, 48.38 ± 15.43 mg l-1 Ca, and 8.20 ± algae are characterized by rapid sinking under calm
2.05 mg l-1 Mg). F. ulna preferred circumneutral pH conditions of thermal stratification and require turbu-
(pH 7.11 ± 0.38) in Alleben Reservoir (Table 5). lence to remain in suspension. This case with regard to
Indeed, WA and CCA indicated that Fragilaria species buoyancy of F. biceps in Alleben Reservoir could be
had preference of higher PO4 value and nearly located supported by the atelomixis pattern.
at spring months than those of other taxa in Alleben Among the chlorophyts, Tetraedron sp., ascribed to
Reservoir during the study period. Preference of functional group of J (Padisák et al., 2003, 2009), had
optimum pH for F. ulna in the present study was also main biovolume peaks in May 2012, September 2012,
found for Synedra ulna (synonym of Fragilaria ulna) and May 2013, after the decreasing of F. biceps
in the stream (Bere & Tundisi, 2009). F. ulna had biovolume. The habitat template for this group is
important biovolume peaks in the spring and autumn, typical of shallow, mixed, and highly enriched
when water mixing periods occurred with enriched systems (including many low-gradient rivers) (Pad-
turbid water in Alleben Reservoir. Water mixing may isák et al., 2009), which mainly corresponds with the
result in drifting of littoral diatoms to the plankton. This characteristics of Alleben Reservoir. As given in
species can be ascribed to the survival strategies of MP Table 5, this species preferred warmer, lower P, and
functional group. The habitat template for this group is softer waters (18.87 ± 3.93°C, 17.96 ± 2.94 lg l-1
typical of frequently stirred up and inorganically turbid PO4, 39.19 ± 13.43 mg l-1 Ca and 7.79 ± 2.30
shallow lakes (Padisák et al., 2009), which corresponds mg l-1 Mg) than that of F. biceps. These results were
with the characteristics of Alleben Reservoir. This also confirmed by CCA (Fig. 5). Tetraedron species
diatom was reported from the artificial and modified was commonly found in Alleben Reservoir, which
lakes in Italy (Tolotti et al., 2010). Fragilaria crotonen- also reported from Mediterranean Reservoirs such as
sis, had important biovolume peaks in the spring during Marathonas Reservoir, Greece (Katsiapi et al., 2011),
the water mixing period in Alleben limno-Reservoir, is Mediterranean reservoirs (Marchetto et al., 2009), and
attributed to P functional group, whose habitat template is Valparaı́so Reservoir, Spain (Negro et al., 2000).
123
130 Hydrobiologia (2014) 740:115–135
The chrysophyte in the phytoplankton of Alleben intolerance of competitors exhausting the carbon.
Reservoir, whose main representative is Dinobryon Lakes well buffered by bicarbonate also make it
divergens, had main biovolume peaks in the beginning difficult for Dinobryon to satisfy its carbon require-
and ending of thermal stratification months. As ment. This being so, the restriction of Dinobryon to
indicated in Table 5, D. divergens developed strongly soft water lakes ought to be inviolable, yet its seasonal
in warm, alkaline, hard water (18.38 ± 4.78°C, pH abundance in Alleben Reservoir is far from being an
7.9 ± 0.46, 45.93 ± 6.39 mg l-1 Ca and 9.24 isolated instance. Others include the karstic Akkaya
± 1.08 mg l-1 Mg). This was intuitively remarkable, spring (Çelekli & Külköylüoğlu, 2007); the deep
given the oft-stated, long-accepted preference of mesotrophic Lake Zagłe˛bocze of Poland with alkaline
Dinobryon spp. for the cool oligotrophic waters water (Solis, 2005); and in the alpine Piburger See in
(Rawson, 1956; Rodhe et al., 1958; Çelekli, 2006). Austria (Tolotti & Thies, 2002).
Chrysophytes were the most important algal group in The dinoflagellate in Alleben Reservoir, Peridini-
oligotrophic Lake Saanajärvi, northern Finland (For- um cinctum, showed its main biovolume peaks in the
sström et al., 2005), as they were reported in the early autumn and summer seasons, when the water
presence of high mountain lakes of Central Europe, column thermal stratification was present. As given in
such as Lake Paione Superiore in Italy (Pugnetti & Table 5, this species preferred warm and slightly
Bettinetti 1999), in a small suburban Lake Strzeszyńs- alkaline water (19.31 ± 6.09°C and pH 8.01 ± 0.37),
kie, Poland (Szela˛g-Wasielewska, 2006), and the which was also confirmed by CCA (Fig. 5). This
oligotrophic mountain lake, Laghetto Inferiore, in species was adapted to warm water and water strat-
Switzerland (Simona et al., 1999). Reynolds et al. ification, which is assigned to the association of Lo
(2002) placed Dinobryon and many smaller chryso- functional group, which is related with summer
phytes in their functional Group E. The habitat epilimnia in mesotrophic lakes (Reynolds et al.,
template for this group is typical of usually small, 2002; Padisák et al., 2009). Peridinium species was
shallow, base poor lakes or heterotrophic ponds also reported from Mediterranean reservoirs (Mar-
(Reynolds et al., 2002; Padisák et al., 2009), which chetto et al., 2009), and a shallow Torrens Lake in the
mainly attributed to the properties of Alleben Reser- South Australia (Regel et al., 2004). Naselli-Flores
voir. Though principally associated with oligotrophic and Barone (2000) highlighted that dinophytes of the
lakes, where their life cycle and low proximal genus Peridinium were among the most important
phosphorus demands provide aids to their survival, it species in two (one natural and one artificial) meso-
was noted that algae of this group are generally absent trophic Sicilian lakes.
from calcareous lakes, yet do frequently occur in Among the crytophytes, Cryptomonas ovata was
calcareous ponds in which there is decomposition of found in Alleben Reservoir during the entire study
organic plant remains or some farm runoff. On the period and had higher biovolume than that of Plagio-
other hand, Dinobryon sociale became briefly abun- selmis nannoplanctica (mainly in spring and autumn).
dant in the calcareous Lake Balaton, following Both small cryptophytes had no important contribution
dredging operations that disturbed the bottom sedi- to total phytoplankton biovolume of Alleben Reservoir.
ment (Reynolds et al., 1993). A capacity for mixotro- Reynolds et al. (2002) and Padisák et al. (2009) reported
phy (some chrysophytes, including Dinobryon, ingest that the small cryptophytes, P. nannoplanctica and C.
bacteria as an additional nutritive source to photo- ovata, were grouped in the X2 (typical of shallow meso-
autotrophy: e.g., previous studies (Bird & Kalff, 1987; eutrophic waters) and the Y (usually small and enriched
Isaksson et al., 1999) may be important to the lakes) functional groups, respectively. Both taxa had
ecological interpretation. The strong suggestion that high biovolume during the mixing period in Alleben
the chrysophytes were starved of carbon and were Reservoir. Becker et al. (2010) reported that these
unable to concentrate carbon from sources other than groups adapted to low light intensity, such as group Y in
carbon dioxide in solution has been verified through a Mediterranean Reservoir.
exhaustive experiments (Saxby-Rouen et al., 1998). Several limno-ecological studies regarding phyto-
The reputation of Dinobryon as an indicator of plankton have been carried out in Mediterranean
oligotrophic conditions was conditioned not by a region (Naselli-Flores, 2003; Moreno-Ostos et al.,
preference for low phosphorus availability but an 2008; Hoyer et al., 2009; Becker et al., 2010; Katsiapi
123
Hydrobiologia (2014) 740:115–135 131
et al., 2011; Molina-Navarro et al., 2014). Very rich recorded during study period. Phytoplankton species
limnosystems are present in Mediterranean region, belong to the functional groups of A, D, E, J, LO, LM,
although knowledge about ecology of the organisms MP, P, and Y as descriptor were evaluated in
with long-term monitoring is generally rather poor phytoplankton composition of Alleben Reservoir.
(Alvarez Cobelas et al., 2005). From that point, the For this reservoir, functional groups of phytoplank-
present study regarding phytoplankton or limno- ton were used as an indicator of trophic state for the
ecology in Alleben Reservoir is the first study of this first time. The study confirmed the potential use of
kind in the southeast of Turkey. The present study the functional groups scheme of phytoplankton for
covered 15 months and resulted that a part of limno- assessing the trophic state and ecological status, and
logical investigations centered on the southeast region provided valuable and complementary information
of Turkey sets out to explain some distinctive features on algal strategies, adaptations, and tolerances to
of the phytoplankton of this Reservoir. Phytoplankton characterize and understand phytoplankton dynamics
biovolume temporally changed, and Cyclotella spe- in the reservoirs. Total phytoplankton biovolume
cies was found to be dominant group in Alleben (9106 lm3 l-1) ranged between 64.3 in October
Reservoir. Nutrient dynamics and light availability 2012 (thermal stratification pattern) and 290.1 in
were mainly driven by the water circulation (stratifi- November 2012 (began water mixing period). Phy-
cation vs. mixing) pattern, governing the phytoplank- toplankton species; the diatom, especially C. plan-
ton dynamics in Alleben Reservoir. This driving force ctonica, C. iris, and F. bicep; the dinoflagellate,
on phytoplankton was also found in Mediterranean Peridinium cinctum; the chlorophyts Tetraedron sp.;
water bodies (Becker et al., 2010; Katsiapi et al., 2011; and the chrysophytes, Dinobryon divergens had
Molina-Navarro et al., 2014). Ecological status of important contribution to the total biovolume. CCA
phytoplankton in Alleben Reservoir was assessed indicated that salinity, temperature, pH, conductiv-
using PTI and Q indices in accordance with Annex V ity, and phosphate were the most important variables
of the WFD (Padisák et al., 2006; EC, 2009; Poikane governing the seasonal succession of phytoplankton
et al., 2011; Phillips et al., 2013). The national species. Multivariate analyses indicated that Cyclo-
assessment systems for phytoplankton in lakes and tella species and C. ovata were mainly found in
reservoirs have been studied in many countries of cooler water, while Peridinium species and C. hirun-
Europe, however, still lack metrics for phytoplankton dinella preferred warmer water during study period.
composition (Poikane, 2009, Birk et al. 2012). From Species of Fragilaria preferred higher PO4 value
that point, the present study will be a contribution to than those of other phytoplankton taxa. Furthermore,
the usage of phytoplankton assemblages as a biolog- Cyclotella species were found in harder water,
ical metric in this region. comparing other phytoplankton taxa. From those
points, the present study regarding phytoplankton or
limno-ecology in Alleben Reservoir is the first study
Conclusions of this kind in the South East of Turkey. Further
studies are needed to resolve some of the curious
Alleben Reservoir was a warm monomictic charac- biological features of warm monomictic Alleben
teristic according to water circulation pattern. This Reservoir that this investigation has revealed. The
reservoir showed characteristic of meso-eutrophic use of multivariate analysis to explore the effects of
with respect to the chlorophyll a and Secchi depth multiple environmental variables on the phytoplank-
that it supported by criteria of OECD and the solution ton is, demonstrably, a powerful means of explora-
of Carlson’s trophic state index. This study also tion of mechanisms and of isolation of the critical
revealed that the suitability of phytoplankton biovo- determinants. The case for invoking the species-
lume, chlorophyll a, phosphate, Secchi depth, PTI, specific biovolumes as an index of importance in the
and Q index were evaluated for assessing the trophic plankton, together with the ascription of the main
state and the ecological status of Alleben Reservoir in components to functional groups, is claimed to
accordance with the EU WFD, OECD, and Carlsons’ provide an important additional dimension in future
solution. A total of 76 counted species in Alleben biomonitoring studies of the reservoir, lake, and
Reservoir belonging to 20 functional groups were other water bodies.
123
132 Hydrobiologia (2014) 740:115–135
Acknowledgements This research was supported by Çelekli, A., 2006. Comparative Analysis of Seasonal Water
TUBITAK (The Scientific and Technical Research Council of Quality Changes and Algae Potential between Lake Abant
Turkey) with the project No: 112Y002. Authors thank to and Lake Gölköy. Ph.D. Thesis, University of Abant İzzet
Scientific Research Projects Executive Council of University of Baysal, Institute of Science.
Gaziantep (FEF.12.01) and Gaziantep water and sewage Çelekli, A. & O. Külköylüoğlu, 2007. On the relationship
management (GASKI). Finally, we thank anonymous editor between ecology and phytoplankton composition in a
and reviewers for valuable comments and suggestions on the karstic spring (Çepni Bolu). Ecological Indicators 7:
manuscript. 497–503.
Dası́, M. J., M. R. Miracle, A. Camacho, J. M. Soria & E.
Vicente, 1998. Summer phytoplankton assemblages across
References trophic gradients in hardwater reservoirs. Hydrobiologia
369/370: 27–43.
Abranthes, N., S. C. Antunes, M. J. Pereira & F. Gonçalves, Dokulil, M. T. & K. Teubner, 2003. Eutrophication and resto-
2006. Seasonal succession of cladocerans and phyto- ration of shallow lakes – the concept of stable equilibria
plankton and their interactions in a shallow eutrophic lake revisited. Hydrobiologia 506(509): 29–34.
(Lake Vela Portugal). Acta Oecologica-International Directive, 2000. Directive 2000/60/EC of the European parlia-
Journal of Ecology 29: 54–64. ment and of the council of 23 October 2000 establishing a
Alvarez Cobelas, M., C. Rojo & D. G. Angeler, 2005. Medi- framework for community action in the field of water
terranean limnology: current status, gaps and the future. policy. Official Journal of the European Communities 327:
Journal of Limnology 64(1): 13–29. 1–72.
APHA AWWA, 1989. Standard methods for the examination of European Communities (EC), 2009. Water Framework Direc-
water and wastewater. 17th ed, American Public Health tive intercalibration technical report. Part 2. In Poikane, S.
Association, Washington D.C. (ed.), Lakes. European Commission, Joint Research Cen-
Babanazarova, O. V. & O. A. Lyashenko, 2007. Inferring long- tre, Ispra.
term changes in the physical–chemical environment of the Ettl, H., 1983. Chlorophyta I Phytomonadina. In Süßwasserflora
shallow enriched Lake Nero from statistical and functional von Mitteleuropa. Band 6 Gustav Fischer Verlag Stuttgart.
analyses of its phytoplankton. Journal of Plankton Forsström, L., S. Sorvari & A. Korhola, 2005. Seasonality of
Research 29(9): 747–756. phytoplankton in subarctic Lake Saanajarvi in NW Finnish
Barbosa, F. A. R. & J. Padisák, 2002. The forgotten lake strat- Lapland. Polar Biology 28: 846–861.
ification pattern: atelomixis, and its ecological importance. Hall, R. I. & J. P. Smol, 1992. A weighted-averaging regression
Verhandlungen Internationaler Verein der Limnologie 28: and calibration model for inferring total phosphorus con-
1385–1395. centration from diatoms in British Columbia (Canada)
Barbosa, L. G., P. M. M. Barbosa & F. A. R. Barbosa, 2011. lakes. Freshwater Biology 27: 417–434.
Vertical distribution of phytoplankton functional groups in Heinonen, P., 1980. Quantity and composition of phytoplankton
a tropical shallow lake: driving forces on a diel scale. Acta in Finnish inland waters. Publications of the Water
Limnologica Brasiliensia 23: 63–73. Research Institute 37: 1–91.
Becker, V., L. Caputo, J. Ordóñez, R. Marcé, J. Armengol, L. Hillebrand, H., C. D. Dürselen, D. Kirschtel, D. Polingher & T.
O. Crossetti & V. L. M. Huszar, 2010. Driving factors of Zohary, 1999. Biovolume calculation for pelagic and
the phytoplankton functional groups in a deep Mediterra- benthic microalgae. Journal of Phycology 35: 403–424.
nean reservoir. Water Research 44(11): 3345–3354. Honti, M., V. Istvánovics & A. Osztoics, 2007. Stability and
Bere, T. & J. G. Tundisi, 2009. Weighted average regression and change of phytoplankton communities in a highly dynamic
calibration of conductivity and pH of benthic diatom environment-the case of large, shallow Lake Balaton
assemblages in streams influenced by urban pollution – São (Hungary). Hydrobiologia 581: 225–240.
Carlos/SP, Brazil. Acta Limnologica Brasiliensia 21(3): Horne, J. A. & C. R. Goldman, 1994. Limnology, 2nd ed.
317–325. McGraw–Hill Inc., New York.
Berlinger, E. G. & D. C. Sigee, 2010. Freshwater Algae. Iden- Hoyer, A. B., E. Moreno-Ostos, J. Vidal, J. M. Blanco, R.
tification and use as Bioindicators, 1st ed. Wiley, London. L. Palomino-Torres, A. Basanta, C. Escot & F. J. Rueda,
Bird, D. F. & J. Kalff, 1987. Algal phagotrophy: regulating 2009. The influence of external perturbations on the
factors and importance relative to photosynthesis in Di- functional composition of phytoplankton in a Mediterra-
nobryon (Chrysophyceae). Limnology and Oceanography nean reservoir. Hydrobiologia 636: 49–64.
32: 277–284. Hutchinson, G. E., 1967. A Treatise on Limnology. Volume II;
Birk, S., W. Bonne, A. Borja, S. Brucet, A. Courrat & S. Poi- Introduction to Lake Biology and the Limnoplankton.
kane, 2012. Three hundred ways to assess Europe’s surface Wiley, New York.
waters: an almost complete overview of biological meth- Isaksson, A., A. K. Bergström, P. Blomqvist & M. Jansson,
ods to implement the Water Framework Directive. Eco- 1999. Bacterial grazing by phagotrophic phytopflagellates
logical Indicators 18: 31–41. in a deep humic lake in northern Sweden. Journal of
Brettum, P., 1989. Alger som indikatorer pa vannkvalitet i Plankton Research 21(2): 247–268.
norske innsjǿer. NIVA Report, Planteplankton. Istvánovic, V., M. Honti, A. Osztoics, H. M. Shafik, J. Padisák,
Carlson, R. E., 1977. A trophic state index for lakes. Limnology Y. Yacobi & W. Eckert, 2005. Continuous monitoring of
and Oceanography 22(2): 361–369. phytoplankton dynamics in Lake Balaton (Hungary) using
123
Hydrobiologia (2014) 740:115–135 133
on-line delayed fluorescence excitation spectroscopy. suitability of derived metrics for assessing the ecological
Freshwater Biology 50: 1950–1970. status in a limno-reservoir, a Water Framework Directive
John, D. M., B. A. Whitton & J. A. Brook, 2002. The Freshwater nondefined type of Mediterranean water body. Lake and
Algal Flora of the British Isles, 1st ed. Cambridge Uni- Reservoir Management 30: 46–62.
versity Press, Cambridge. Moreno-Ostos, E., L. Cruz-Pizarro, A. Basanta & D. G. George,
Juggins, S. & C. F. J. ter Braak, 1992. CALIBRATE-Program 2008. The spatial distribution of different phytoplankton
for species-environment calibration by (weighted averag- functional groups in a Mediterranean reservoir. Aquatic
ing) partial least squares regression. Environmental Ecology 42: 115–128.
Change Research Centre, University College London, Naselli-Flores, L., 1999. Limnological aspects of Sicilian res-
London. ervoirs: a comparative, ecosystem approach. In Tundisi, J.
Katsiapi, M., M. Moustaka-Gouni, E. Michaloudi & K. G. & M. Straškraba (eds), Theoretical Reservoir Ecology
A. Kormas, 2011. Phytoplankton and water quality in a and its Applications. Backhuys, Kerkwerve: 283–311.
Mediterranean drinking-water reservoir (Marathonas Res- Naselli-Flores, L., 2003. Man-made lakes in Mediterranean
ervoir, Greece). Environmental Monitoring and Assess- semiarid climate: the strange case of Dr Deep Lake and Mr
ment 181: 563–575. Shallow Lake. Hydrobiologia 506–509: 13–21.
Komárek, J. & K. Anagnostidis, 1998. Cyanoprokaryota Naselli-Flores, L. & R. Barone, 2000. Phytoplankton dynamics
Chroococcales. In Susswasserflora von Mitteleuropa. and structure: a comparative analysis in natural and man-
Gustav Fisher, Jena. made water bodies of different tropic state. Hydrobiologia
Komárek, J. & B. Fott, 1983. Chlorophyceae (Grünalgen) 438: 65–74.
Ordnung: Chlorococcales. In Huber–Pestallozi – Das Naselli-Flores, L. & R. Barone, 2007. Pluriannual morpholog-
Phytoplankton des Süßwassers Systematik und Biologie 7 ical variability of phytoplankton in a highly productive
Teil, 1 Hälfte E Schweizerbart‘sche Verlagsbuchhandlung, Mediterranean reservoir (Lake Arancio, Southwestern
Stuttgart. Sicily). Hydrobiologia 578: 87–95.
Krammer, K. & H. Lange-Bertalot, 1991a. Bacillariophyceae. 3 Naselli-Flores, L. & R. Barone, 2011. Invited review – fight on
Teil: Centrales, Fragilariaceae, Eunotiaceae. In Ettl, plankton or, phytoplankton shape and size as adaptive tools
H., J. Gerloff, H. Heynig & D. Mollenhauer (Hrsgb.), to get ahead in the struggle for life. Cryptogamie Algologie
Süßwasserflora von Mitteleuropa. Band 2. Fischer Verlag, 32(2): 157–204.
Stuttgart. Negro, A. I., C. De Hoyos & J. C. Vega, 2000. Phytoplankton
Krammer, K. & H. Lange-Bertalot, 1991b. Bacillariophyceae. 4 structure and dynamics in Lake Sanabria and Valparáıso
Teil: Achnanthaceae. Kritische Erganzungen zu Navicula reservoir (NW Spain). Hydrobiologia 424: 25–37.
(Lineolatae) und Gomphonema. In Ettl, H., G. Gartner, J. Padisák, J., J. Köhler & S. Hoeg, 1999. The effect of changing
Gerloff, H. Heynig & D. Mollenhauer (eds), Süßwasserfl- flushing rates on development of late summer Aphani-
ora von Mitteleuropa. Band 2. Fischer Verlag, Stuttgart. zomenon and Microcystis populations in a shallow lake,
Krammer, K. & H. Lange–Bertalot, 1999a. Bacillariophyceae. 1 Müggelsee, Berlin, Germany. In Tundisi, J. G. & M.
Teil: Naviculaceae. In Ettl, H., J. Gerloff, H. Heynig & D. Straškraba (eds), Theoretical Reservoir Ecology and its
Mollenhauer (eds), Süßwasserflora von Mitteleuropa. Applications. Backhuys, The Netherlands: 411–424.
Band 2. Akademischer Verlag, Heidelberg, Berlin. Padisák, J., G. Borics, G. Fehér, I. Grigorszky, I. Oldal, A.
Krammer, K. & H. Lange–Bertalot, 1999b. Bacillariophyceae. 2 Schmidt & Z. Zámbóné-Doma, 2003. Dominant species,
Teil: Bacillariaceae, Epithemiaceae, Surirellaceae. In Ettl, functional assemblages and frequency of equilibrium phases
H., J. Gerloff, H. Heynig & D. Mollenhauer (eds), Süß- in late summer phytoplankton assemblages in Hungarian
wasser-flora von Mitteleuropa. Band 2. Akademischer small shallow lakes. Hydrobiologia 502: 157–168.
Verlag, Heidelberg, Berlin. Padisák, J., G. Borics, I. Grigorszky & É. Soróczki-Pintér, 2006.
Kruk, C., N. Mazzeo, G. Lacerot & C. S. Reynolds, 2002. Use of phytoplankton assemblages for monitoring ecologi-
Classification schemes for phytoplankton: a local valida- cal status of lakes within the Water Framework Directive:
tion of a functional approach to the analysis of species the assemblage index. Hydrobiologia 553(1): 1–14.
temporal replacement. Journal of Plankton Research 24(9): Padisák, J., L. O. Crossetti & L. Naselli-Flores, 2009. Use and
901–912. misuse in the application of the phytoplankton functional
Leps, J. & P. Smilauer, 2003. Multivariate analysis of ecological classification: a critical review with updates. Hydrobiolo-
data using CANOCO Cambridge University Press, gia 621: 1–19.
Cambridge. Padisák, J., E. Hajnal, L. Naselli-Flores, M. T. Dokulil, P. Nõges
Marchetto, A., B. M. Padedda, M. A. Mariani, A. Lugliè & N. & T. Zohary, 2010. Convergence and divergence in orga-
Sechi, 2009. A numerical index for evaluating phyto- nization of phytoplankton communities under various
plankton response to changes in nutrient levels in deep regimes of physical and biological control. Hydrobiologia
Mediterranean reservoirs. Journal of Limnology 68: 639: 205–220.
106–121. Phillips, G., A. Lyche-Solheim, B. Skjelbred, U. Mischke, S.
Molina-Navarro, E., A. Sastre-Merlı́n Martı́nez-Perez & D. M. Drakare, G. Free, M. Järvinen, C. de Hoyos, G. Morabito,
del Pozo, 2012. The limnological characteristics and zoo- S. Poikane, et al., 2013. A phytoplankton trophic index to
plankton community of a newly created site: the Pareja assess the status of lakes for the Water Framework Direc-
Limno-reservoir. Limnetica 31(1): 95–106. tive. Hydrobiologia 704: 75–95.
Molina-Navarro, E., S. Martı́nez-Perez, A. Sastre-Merlı́n, M. Poikane, S., M. V. D. Berg, J. Ortiz-Casas, G. Phillips, A.
Verdugo-Althöfer & J. Padisák, 2014. Phytoplankton and L. Solheim, D. Tierney & G. Wolfram, 2009. Lake
123
134 Hydrobiologia (2014) 740:115–135
assessment strategy in European Union (EU): case study of Salmaso, N., 2002. Ecological patterns of phytoplankton
European large lakes. Verh International Verein Limnol- assemblages in Lake Garda: seasonal, spatial and historical
ogy 30: 1007–1012. features. Journal of Limnology 61(1): 95–115.
Poikane, S., M. van den Berg, S. Hellsten, C. de Hoyos, J. Ortiz- Salmaso, N. & J. Padisák, 2007. Morpho-functional groups and
Casas, K. Pall, R. Portielje, G. Phillips, A. L. Solheim, D. phytoplankton development in two deep lakes (Lake
Tierney, et al., 2011. Lake ecological assessment systems Garda, Italy and Lake Stechlin, Germany). Hidrobiologia
and intercalibration for the European Water Framework 578: 97–112.
Directive: aims, achievements and further challenges. Saros, J. E., T. J. Michel, S. J. Interlandi & A. P. Wolfe, 2005.
Procedia Environmental Sciences 9: 153–168. Resource requirements of Asterionella formosa and
Popovsky, J. & L. A. Pfiester, 1990. Dinophyceae (Dinoflag- Fragilaria crotonensis in oligotrophic alpine lakes:
ellida). In Süßwasserflora von Mitteleuropa. Band 6. implications for recent phytoplankton community reorga-
Gustav Fischer Verlag, Jena. nizations. Canadian Journal of Fisheries and Aquatic Sci-
Pugnetti, A. & R. Bettinetti, 1999. Biomass and species structure ences 62: 1681–1689.
of the phytoplankton of a high mountain lake (Lake Paione Saxby-Rouen, K. J., B. S. C. Leadbeater & C. S. Reynolds, 1998.
Superiore, Central Alps, Italy). Journal of Limnology 58: The relationship between the growth of Synura petersenii
127–130. (Synurophyceae) and the components of the dissolved
Rakocevic-Nedovic, J. & H. Hollert, 2005. Phytoplankton inorganic system. Phycologia 37: 467–477.
community and chlorophyll a as trophic state indices of Simona, M., A. Barbieri, M. Veronesi, S. Malusardi & V.
Lake Skadar (Montenegro, Balkan). Environmental Sci- Straskrábová, 1999. Seasonal dynamics of plankton in a
ence and Pollution Research 12(3): 146–152. mountain lake in the Southern Alps (Laghetto Inferiore,
Rawson, D. S., 1956. Algal indicators of trophic lake types. Switzerland). Journal of Limnology 58: 169–178.
Limnology and Oceanography 1: 18–25. Solis, M., 2005. Relationships between selected abiyotic vari-
Reynolds, C. S., 1980. Phytoplankton assemblages and their ables and phytoplankton composition in deep mesotrophic
periodicity in stratifying lake system. Holarctic Ecology 3: Lake Zaglebocze. Oceanological and Hydrobiological
141–159. Studies 19(4): 81–96.
Reynolds, C. S., 1984. Phytoplankton periodicity. Interactions Soares, M. C. S., M. M. Marinho, V. L. M. Huszar, C. W. C.
among form, function and environmental variability. Branco & S. M. F. O. Azevedo, 2008. The effects of water
Freshwater Biology 14: 111–142. retention time and watershed features on the limnology of
Reynolds, C. S., 1997. Vegetation Processes in the Pelagic: A two tropical reservoirs in Brazil. Lakes & Reservoirs:
Model for Ecosystem Theory. Ecology Institute, Olden- Research and Management 13: 257–269.
dorf/ Luhe: 371. Souza, M. B. G., C. F. A. Barros, F. Barbosa, É. Hajnal & J.
Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cam- Padisák, 2008. Role of atelomixis in replacement of phy-
bridge University Pres, Cambridge. toplankton assemblages in Dom Helvécio Lake, South-
Reynolds, C. S., J. Padisák & I. Kóbor, 1993. A localized bloom East Brazil. Hydrobiologia 6007: 211–224.
of Dinobryon sociale in Lake Balaton: Some implications Stoermer, E. F. & J. P. Smol, 1999. The Diatoms: Applications
for the perception of patchiness and the maintenance of for the Environmental and Earth Sciences. Cambridge
species richness. Abstracta Botanica 17: 251–260. University Press, Cambridge, UK.
Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Straškraba, M. 1999. Retention time as a key variable of res-
Melo, 2002. Towards a functional classification of the ervoir limnology. In Theoretical reservoir ecology and its
freshwater phytoplankton, review. Journal of Plankton applications. In Tundisi, J. G. & M. Straskraba (eds),
Research 24(5): 417–428. International Institute of Ecology, Brazilian Academy of
Rodhe, W., R. A. Vollenweider & A. Nauwerck, 1958. The Sciences and Backhuys Publishers, Leiden: 385–410.
primary production and standing crop of phytoplankton. In Sun, J. & D. Liu, 2003. Geometric models for calculating cell
Buzzati-Traverso, A. A. (ed.), Perspectives in Marine biovolume and surface area for phytoplankton. Journal of
Biology. University of California Press, Berkeley. Plankton Research 25: 1331–1346.
Rott, E., 1981. Some results from phytoplankton counting in- Szela˛g-Wasielewska, E., 2006. Trophic status of lake water
tercalibrations. Schweiz Z. Hydrologie 43: 34–62. evaluated using phytoplankton community structure –
Rott, E., 1984. Phytoplankton as biological parameter for the change after two decades. Polish Journal of Environmental
trophic characterization of lakes. Verhandlungen des In- Studies 15(1): 139–144.
ternationalen Verein Limnologie 22: 1078–1085. ter Braak, C. J. F., 1995. Ordination. In Jongman, R. H. G., C.
Rott, E., 1991. Methodological aspects and perspectives in the J. F. ter Braak & O. F. R. Van Tongeren (eds), Data Ana-
use of periphyton for monitoring and protecting rivers. In lysis in Community and Landscape Ecology. Cambridge
Whitton, B. A., E. Rott & G. Friedrich (eds), Use of Algae University Press, Cambridge.
for Monitoring Rivers. E. Rott, Institüt für Botanik, Univ. ter Braak, C. J. F. & P. Smilauer, 1998. CANOCO Reference
Innsbruk, Innsbruk: 9–16. Manual and User’s Guide to CANOCO for Windows
Regel, R. H., J. D. Brookes & G. G. George, 2004. Vertical (Version 4). Center for Biometry, Wageningen.
migration, entrainment and photosynthesis of the fresh- Tolotti, M. & H. Thies, 2002. Phytoplankton community and
water dinoflagellate Peridinium cinctum in a shallow urban limnochemistry of Piburger See (Tyrol Austria) 28 years
lake. Journal of Plankton Research 26: 143–157. after lake restoration. Journal of Limnology 61(1): 77–88.
123
Hydrobiologia (2014) 740:115–135 135
Tolotti, M., F. Corradini, A. Boscaini & D. Calliari, 2007. Wehr, J. D. & R. G. Sheath, 2003. Freshwater Algae of North
Weather-driven ecology of planktonic diatoms in Lake America: Ecology and Classification. Academic Press, San
Tovel (Trentino, Italy). Hydrobiologia 578: 147–156. Jose.
Tolotti, M., A. Boscaini & N. Salmaso, 2010. Comparative Wetzel, R. G. & G. E. Likens, 2000. Limnological Analyses, 3rd
analysis of phytoplankton patterns in two modified lakes ed. Springer, Berlin.
with contrasting hydrological features. Aquatic Sciences Willén, E., 2000. Phytoplankton in water quality assessment-An
72: 213–226. indicator concept. In Heinonen, P., G. Ziglio & A. Van der
Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Beken (eds), Hydrological and Limnological Aspects of
phytoplankton-methodik. Mitteilungen Internationale Lake Monitoring. Wiley, New York: 58–80.
Vereinigung Theoretische und Angewandte Limnologie Youngman, R. E., 1978. Measurement of Chlorophyll a Water
9: 1–38. Research Center. Tech Rap Tr-82. Water Research Center,
Vollenweider, R. A. & J. Kerekes, 1982. Eutrophication of New York.
Waters, Monitoring, Assessment and Control. OECD Zohary, T., J. Padisák & L. Naselli-Flores, 2010. Phytoplankton
Cooperative Programme on Monitoring of Inland Waters in the physical environment: beyond nutrients, at the end,
(Eutrophication Control). OECD, Paris. there is some light. Hydrobiologia 639: 261–269.
123